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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 8  |  Issue : 2  |  Page : 132-137

Evaluation of GeneXpert Mycobacterium tuberculosis/Rifampin for the detection of Mycobacterium tuberculosis complex and rifampicin resistance in nonrespiratory clinical specimens


TB Unit, Pathology and Genetics Department, Rashid Hospital, Dubai, UAE

Date of Web Publication14-Jun-2019

Correspondence Address:
Maya Habous
TB Unit, Pathology and Genetics Department, Rashid Hospital, Dubai
UAE
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmy.ijmy_83_19

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  Abstract 


Background: The objective of this study is to assess the performance of Xpert Mycobacterium tuberculosis (MTB)/rifampin (RIF), an automated molecular test for MTB and resistance to RIF, against smear microscopy and culture method for the diagnosis of MTB infection. Methods: This is a retrospective analysis of 168 nonrespiratory patient specimens suspected of tuberculosis (TB) at TB Laboratory of Dubai Health Authority in the United Arab Emirates between September 2016 and November 2018. Each sample underwent smear microscopy, mycobacterial culture, and GeneXpert MTB/RIF test. Results: Of 168 nonrespiratory samples, 52 samples were positive by both culture and Xpert MTB/RIF, 9 samples were detected positive only by culture. Sensitivity, specificity, positive predictive value, and negative value of the Xpert MTB/RIF test were 82.69%, 100%, 100%, and 92.80%, respectively. No false positive was yielded by the Xpert MTB/RIF, and all 116 samples were true negative by Xpert MTB/RIF. The sensitivity of the Xpert MTB/RIF was 76.92% in lymph node tissue and aspirates, 66.67% in cerebrospinal fluid, 100% in gastric lavage and aspirate, 81.25% in other body fluids, 100% in pus, 85.71% in urine, and 66.67% in other tissue samples. Of 168 strains, five strains were rifampicin resistant by phenotypic and Xpert MTB/RIF and 163 were susceptible to rifampicin with culture and Xpert MTB/RIF. Conclusion: The performance of Xpert MTB/RIF assay was comparable to the gold standard culture method for identification of MTB in nonrespiratory clinical specimens. It does not replace the gold standard culture method, but it helps to achieve better sensitivity and obtain rapid results within 2 h.

Keywords: Extrapulmonary tuberculosis, GeneXpert Mycobacterium tuberculosis/rifampin, Mycobacterium tuberculosis complex, resistance to rifampicin


How to cite this article:
Habous M, E. Elimam MA, Kumar R, L. Deesi ZA. Evaluation of GeneXpert Mycobacterium tuberculosis/Rifampin for the detection of Mycobacterium tuberculosis complex and rifampicin resistance in nonrespiratory clinical specimens. Int J Mycobacteriol 2019;8:132-7

How to cite this URL:
Habous M, E. Elimam MA, Kumar R, L. Deesi ZA. Evaluation of GeneXpert Mycobacterium tuberculosis/Rifampin for the detection of Mycobacterium tuberculosis complex and rifampicin resistance in nonrespiratory clinical specimens. Int J Mycobacteriol [serial online] 2019 [cited 2019 Jul 15];8:132-7. Available from: http://www.ijmyco.org/text.asp?2019/8/2/132/260390




  Introduction Top


The World Health Organization (WHO's) global tuberculosis (TB) report 2018 stated that TB causes 10 million cases and 1.3 million deaths annually and it is estimated that 3.6 million cases are either not detected or not notified to public health services each year. TB is one of the most significant contagious pathogens in the world and considered one of the top 10 causes of death worldwide.[1] This aerobic organism is transmitted through inhalation of particles produced by coughing, sneezing, or by close contact with infected people. The global priorities for TB care and control are to improve case-detection and to detect cases earlier, including cases of the smear-negative disease, which are often associated with co-infection with the human immunodeficiency virus and young age, and to enhance the capacity to diagnose multidrug-resistant TB (MDR-TB).[2],[3] The development of MDR-TB, defined as resistance to at least isoniazid and rifampin (RIF) represents a public health concern and threatens global TB control programs.[4]

Laboratory confirmed the diagnosis of active TB is pivotal for the management of disease and is an effective public health intervention.

The current gold standard for confirmation of TB is mycobacterial culture, which is both labor-intensive and time-consuming; it may take up to 8 weeks to confirm the diagnosis. Although smear microscopy is a simple and rapid method for the detection of Mycobacterium tuberculosis (MTB), it lacks sensitivity and requires multiple sputum samples. Genotypic methods have considerable advantages in terms of scaling up the programmatic management and surveillance of drug-resistant TB, offering quicker diagnosis, standardized testing, the potential for high throughput, and having fewer requirements for ensuring laboratory biosafety.[3]

The WHO has recommended a number of molecular diagnostic devices for rapid diagnosis of MTB. The Xpert MTB/RIF test is recommended as the initial diagnostic test for patients being evaluated for pulmonary and extrapulmonary TB.[5] This can result in more bacteriologically confirmed cases and shortened time to treatment. The assay detects MTBas well as mutation that confer rifampicin resistance using three specific primers and five unique molecular probes to ensure a high degree of specificity. It provides results directly from specimens in <2 h. When the assay detects MTBwith rifampicin resistance, clinicians will enrol patient on a treatment regimen requiring second-line drugs instead of first-line drugs.[3]

It remains the only fully automated cartridge-based nucleic acid amplification test. The test can detect both TB and resistance to rifampicin in <2 h, and it is the only mature technology representing a new generation of automated platforms for molecular diagnosis.[6]

While the performance of Xpert MTB/RIF in the detection of MTB complex in respiratory samples is well described, its performance in extrapulmonary (nonrespiratory) clinical specimens has not been well characterized with lower sensitivity and specificity in some studies.[7],[8]

Extrapulmonary MTB infection remains a diagnostic challenge not only due to the low number of bacteria but also due to invasive procedures often required for sample collection. The TB of the lymph nodes (TB lymphadenitis) is one of the most common forms of extrapulmonary TB whose diagnosis still faces many challenges.[9]

In October 2013, the WHO issued updated policy guidance providing revised recommendations on using Xpert MTB/RIF to diagnose pulmonary TB, pediatric TB, extrapulmonary TB, and rifampicin resistance.[10] This decision was based on emerging evidence from a meta-analysis of 85 peer-reviewed publications that Xpert MTB/RIF performed favorably in detecting extrapulmonary infections including lymph nodes, cerebrospinal fluid (CSF), and body fluids. Specifically, in the pediatric age group, where up to 60% of patients with extrapulmonary TB develop cervical lymphadenitis.[8] The global burden of TB in children was estimated to be 500,000 cases, representing approximately 6% of all cases of TB.[10] Furthermore, since the diagnosis of MTB in children is often delayed due to nonspecific clinical features and difficult expectoration, and to the difficulties associated with obtaining microbiological confirmation of the diagnosis of TB in children.[11] The Xpert MTB/RIF assay stands out as a useful method in the diagnosis of pediatric MTB. These recommendations are consistent with another meta-analysis in which 27 peer-reviewed publications collectively suggest that Xpert MTB/RIF accurately detects extrapulmonary TB in children and adults.[10],[11],[12]

The aim was to evaluate the Xpert MTB/RIF test in diagnosing extrapulmonary TB.


  Methods Top


Study type, population, and sampling

This is a retrospective study from September 2016 to November 2018 at TB Laboratory of Dubai Health Authority, UAE. It included inpatients and outpatients presenting with suspected extrapulmonary TB from 4 hospitals and all public health centers in Dubai. The patient's extrapulmonary samples suspected of TB were included in our evaluation. The extrapulmonary samples (n = 168) with 97 males and 71 females [Figure 1], includes tissue, aspirates, pus in addition to biological fluids [Figure 2].
Figure 1: Patient sex group distribution

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Figure 2: Sampling distribution

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Isolation and identification of Mycobacterium

The nonrespiratory specimens, including tissue, aspirates, biological fluids, and pus, were processed using the standard N-acetyl-L-cysteine decontamination and concentration method. Tissues and biopsies were first, grinded firmly with a small amount of sterile saline by a tissue grinder (Omni Bead Ruptor), and then processed similar to other specimens. Freshly prepared Mycoprep™ NALC-NaOH solution (Becton Dickinson, Sparks, MD, USA) was added to the specimen at equal volume (1:1), mixed on vortex, and left for 15 min for digestion at room temperature. A double amount (twice the amount of mixture) of sterile phosphate buffer (pH 6.8) (Becton Dickinson, Sparks, MD, USA) was then added to the mixture and centrifuged for 15 min at 3000 rpm. The supernatant was then removed, and the sediment was dissolved in 2.5 ml of sterile phosphate buffer for further study. Decontamination was not required for sterile specimens such as CSF, synovial fluid, pleural fluid, pericardial fluid, peritoneal fluid, ascetic fluid, and other sterile fluids. Since sterility is not always guaranteed, it was always recommended to streak a drop of the resuspended sediment on blood agar. If there was growth in blood agar, then decontamination was performed in the next day, where the sediment was resuspended processed similar to sputum samples.

Each sample was processed for smear microscopy by Ziehl-Neelsen and Auramine-O stains and conventional cultured in both MGIT Bactec 960 liquid medium (Becton Dickinson Microbiology System, USA) and Löwenstein-Jensen solid media (Becton Dickinson BBLTM Prepared Culture Media). Identification of MTB isolated from solid or liquid cultures by immune chromatographic assay for rapid species identification (Becton Dickinson MGITTM TBC Identification Test). Phenotypic culture-based drug susceptibility testing methods on MGIT 960 (Becton Dickinson Microbiology System, USA), using the WHO recommended critical concentrations, were the reference standards for rifampicin resistance.[13]

GeneXpert Mycobacterium tuberculosis/rifampin

The Xpert MTB/RIF real-time polymerase chain reaction assay was performed in accordance with the manufacturer's instructions described in the package insert and with Xpert MTB/RIF implementation manual/WHO/2014.[3] Briefly, clinical samples except CSF were added to sample reagents after processing (either digestion, decontamination and concentration for biopsy, pus, urine, gastric lavage, and nonsterile fluid samples or concentration after centrifugation for sterile fluid samples) using a ratio of (1:2) by adding a double volume of the Xpert MTB/RIF Sample Reagent (1.4 ml)–(0.7 ml) of concentrated pellet, after vortexing and 15 min incubation at room temperature, 2 ml of the processed specimen were added to the Xpert MTB/RIF cartridge. For CSF, where the minimum volume of sample required was 3 ml, the entire specimen was transferred to a conical centrifuge tube, and concentrated the specimen at 3000 g for 15 min; then, the deposit was resuspended into a final volume of 2 ml by adding the Xpert MTB/RIF sample reagent. Two milliliters of the concentrated CSF specimen were transferred to the Xpert MTB/RIF cartridge that was loaded into the Xpert machine.

Statistical analysis

Data were analyzed with the Excel® software. The number of true positives (tp), true negatives (tn), false positives (fp), and false negatives (fn) were calculated on a per sample basis and entered into 2 × 2 tables. Sensitivity and specificity were calculated based on these tables as tp/(tp + fn) and tn/(tn + fp), respectively. Positive predictive value was equal to (tp) reported on total positive, and negative predictive value (NPV) was equal to (tn) reported on the total negative.

This study was approved by the Dubai Scientific Research Ethics Committee of Dubai Health Authority (Ref: DSREC-03/2019_07) and was performed in accordance with all national regulations.


  Results Top


A total of 168 samples were included in the study, with 97 males (57.74%) and 71 females (42.26%) [Figure 1]. The distribution of 168 samples is shown in the below flowchart [Figure 2]. Mostly, the samples are from biological fluids 59.52%(100/168), from tissues and aspirate 23.80% (40/168), and from pus it is 16.68%(28/168).

GeneXpert sensitivity and specificity results were compared to culture used as a reference standard. Of the 168 samples processed, 52 (30.95%) yielded MTBby culture (liquid and/or solid), whereas 116 remained negative.

Of 52 culture positive, 35 nonrespiratory samples were smear positive, compared to culture results, the sensitivity of smear examination was only 67.31% (35/52) with 100% (116/116) specificity.

Of 52 culture positive, 43 samples were MTB detected by Xpert MTB/RIF, compared to culture results, the sensitivity of Xpert MTB/RIF was 82.69% (43/52) with 100% (116/116) specificity. For the 35 smear-positive samples, Xpert MTB/RIF detected MTB consistently in all the 35 with a sensitivity of 100%, and culture detected MTB in all 35 samples [Table 1] and [Table 2].
Table 1: The specimens analyzed for Mycobacterium tuberculosis complex detection by smear examination, GeneXpert Mycobacterium tuberculosis/rifampin and culture

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Table 2: The sensitivity and specificity of the smear examination and GeneXpert Mycobacterium tuberculosis/rifampin in diagnosing extrapulmonary tuberculosis and rifampicin resistant compared against culture as a reference standard

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Among the 133 smear-negative nonrespiratory samples, MTB was confirmed in 17 samples, the eight samples were positive, both by culture and the Xpert MTB/RIF assay, and 9 samples were positive only by culture, the remaining 116 samples were negative, both by culture and the Xpert MTB/RIF assay. The sensitivity of the Xpert MTB/RIF test depended on the smear examination results. We observed 100% (35/35) sensitivity for patients with positive smears and 93.92% (125/133) sensitivity for patients with negative smears.

The Xpert MTB/RIF yielded no fp and 116 samples were tn with the specificity of 100% and a NPV of 92.8%. Compared to culture, the sensitivity of smear examination was only 67.31% (35/52), while it was increased to 82.69% (43/52) with Xpert MTB/RIF assay in our evaluation. The total performance of smear microscopy and the Xpert MTB/RIF assay compared to culture used as reference standard [Table 2].

The sensitivity of the Xpert MTB/RIF was 76.92% (10/13) in lymph node tissue and aspirates, 66.67% (2/3) in CSF, 100% (1/1) in gastric lavage and aspirate, 81.25% (13/16) in body fluids, 100% (9/9) in pus, 85.71% (6/7) in urine, and 66.67% (2/3) in other tissue samples.

Detection of rifampin resistance

Five samples were RIF resistance with Xpert MTB/RIF assay, 2 pus, 2 body fluid, and 1 urine samples all the 5 samples showed RIF resistant by both phenotypic and genotypic detection methods. The remaining 163 samples were RIF sensitive by phenotypic in culture and genotypic by Xpert MTB/RIF assay.


  Discussion Top


While a number of studies assessed the Xpert MTB/RIF assay in different populations, there are only limited data in the Gulf countries.[14],[15],[16] Various studies have confirmed the use of the GeneXpert MTB/RIF assay in diagnosing TB from various types of nonrespiratory samples with varying sensitivities (52%–100%) and specificities (86%–100%)[17],[18],[19]

The sensitivity of smear microscopy was found to be 67.31% (35/52 specimens) in our study, higher than other studies of 51% reported by Vadwai et al.,[20] 33.3% reported by Al-Ateah et al.,[14] and 28.6% reported by Malbruny et al.[21]

The sensitivity of Xpert MTB/RIF in our study was 82.69%, compared to the sensitivity of 83% reported by Vadwai et al.,[20] 94.4% by Al-Ateah et al.,[14] 85.7% reported by Malbruny et al.,[21] 75% reported by Zmak et al.,[22] and 82.3% reported by Bajrami et al.[23] We found that the Xpert MTB/RIF assay substantially increased MTB detection with higher sensitivity in smear-positive (100%) than smear-negative patients (94.32) which is also higher than the 64% reported by Vadwai et al.,[20] 81.2% reported by Marouane et al.,[24] 70% reported by Zmak et al.[22] and 48% reported by Das et al.[25]

Introducing the Xpert MTB/RIF assay early in the diagnostic workflow can potentially improve detection and shorten turn-around time in the laboratory. Recent reports suggest that Xpert MTB/RIF assay increases the rate of detection of RIF resistance, decreases unnecessary empiric treatment among smear-negative extrapulmonary TB and increases the early initiation of second-line drugs treatment.[26] In our evaluation, the Xpert MTB/RIF assay correctly detected the rpo B gene mutation associated with RIF-resistance in two samples of pus, two samples of body fluids, and one sample of urine. Therefore, the sensitivity and specificity of the Xpert MTB/RIF assay for the detection of RIF-resistant MTB were 100%, compared to the sensitivity of 100% reported by Kim et al.[27]

We found that the Xpert MTB/RIF assay performs well in detecting extrapulmonary TB from different sites. The sensitivity was 76.92% in lymph nodes and aspirates, 66.67% in other tissues and 66.67% in CSF in our study, as compared with 84.9%, 81.2%, and 79.5%, respectively, in meta-analysis of the sensitivity of Xpert MTB/RIF in diagnosing extrapulmonary TB compared against culture as a reference standard.[7] In our study, the sensitivity in lymph nodes was lower than that reported by A. Ghariani et al. (94.9%).[9] The sensitivity was 81.25% in body fluids, 100% in pus in our study, as compared with 76% and 96%, respectively, in Vadwai et al.[20]

The study has shown that the GeneXpert MTB/RIF assay has good sensitivity (77%–100%) for specimens such as body fluid, lymph node tissue and aspirate, pus, urine, and moderate (66%) sensitivity for CSF and other tissues in our setting.


  Conclusion Top


The results of our evaluation are consistent with the existing data and enhance the performance of Xpert MTB/RIF assay in detection of MTB in nonrespiratory samples in TB Laboratory, Dubai Health Authority/UAE patients. We provide further evidence that the Xpert MTB/RIF system has superior sensitivity and specificity, which can positively impact clinical outcomes. Xpert MTB/RIF allows accurate and early diagnosis of TB infection and the shorter turnaround time provides an opportunity for timely therapeutic intervention, which is beneficial not only for the patient but also for any possible contacts. Our findings support recent WHO guidelines regarding the use of XpertMTB/RIF for extrapulmonary diagnosis from nonrespiratory samples.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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World Health Organization. Global Tuberculosis Report 2018. (WHO/CDS/TB/2018.20. Geneva: World Health Organization; 2018. Available from: http://apps.who.int/iris/bitstream/handle/10665/274453/9789241565646-eng.pdf?ua=1. [Last accessed on 2018 Sep 20].  Back to cited text no. 1
    
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[PUBMED]  [Full text]  
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