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 Table of Contents  
Year : 2020  |  Volume : 9  |  Issue : 4  |  Page : 397-404

Performance of Xpert MTB/RIF in comparison with light-emitting diode-fluorescence microscopy and culture for detecting tuberculosis in pulmonary and extrapulmonary specimens in Bamako, Mali

1 University Clinical Research Center-SEREFO Laboratory, University of Sciences, Techniques and Technologies of Bamako, Bamako, Mali
2 Department of Public Health, Faculty of Medicine and Dentistry, USTTB, Bamako, Mali
3 University Clinical Research Center-SEREFO Laboratory, University of Sciences, Techniques and Technologies of Bamako, Bamako, Mali; Department of Medical Biochemistry, School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa
4 Department of National Reference TB Laboratory, National Institute of Public Health (INSP), Bamako, Mali
5 University Clinical Research Center-SEREFO Laboratory, University of Sciences, Techniques and Technologies of Bamako, Bamako, Mali; Center of Global Health, Northwestern University, Chicago, IL, USA
6 Collaborative Clinical Research Branch, Division of Clinical Research, NIAID/NIH, Bethesda, MD, USA
7 Department of Laboratory Medicine and Hospital Hygiene Services, University Teaching Hospital of Point G, Bamako, Mali

Date of Submission09-Sep-2020
Date of Decision29-Sep-2020
Date of Acceptance03-Oct-2020
Date of Web Publication15-Dec-2020

Correspondence Address:
Diarra Bassirou
University Clinical Research Center.SEREFO Laboratory, University of Sciences, Techniques and Technologies of Bamako, Bamako
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijmy.ijmy_171_20

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Background: The diagnosis of tuberculosis (TB) has mostly been relied on a long-used method called sputum smear microscopy. In 2010, Xpert MTB/RIF assay was approved by the World Health Organization for simultaneous TB diagnosis and detection of resistance. Our current study was undertaken to compare the diagnostic performance of Xpert MTB/RIF assay to auramine staining-based light-emitting diode-Fluorescence Microscopy (LED-FM) considering culture as the gold standard method for pulmonary and extrapulmonary TB. Method: Pulmonary and extrapulmonary specimens of suspected TB patients were examined in this study. From January 2016 to June 2019, sputum, urine, superficial swabs, gastric aspirates, and pleural infusion specimens were collected from new and previously treated TB individuals. Specimens were examined using Xpert MTB/RIF, LED-FM, and Mycobacterium culture techniques to evaluate their performance. Results: A total of 697 suspected TB samples were included in this analysis, and of these, 469 (67.29%) were positive for all three used methods. The overall sensitivities, specificities, and positive and negative predictive values were 99.6%, 62.0%, 88.4%, and 98.2% for Xpert MTB/RIF and 88.0%, 95.6%, 99.0%, and 60.7% for LED-FM, respectively, compared to culture method. Conclusion: The sensitivity of Xpert MTB/RIF assay was observed to be higher than the LED-FM method, thus suggesting this molecular technique as a promising tool for the diagnosis of pulmonary and extrapulmonary TB, which will help in the management of TB infections in developing countries such as Mali.

Keywords: Bamako, culture, light-emitting diode fluorescent microscopy, Mali, Xpert MTB/RIF

How to cite this article:
Combo Georges TA, Aissata T, Fatimata D, Abou CC, Gagni C, Moise SA, Boureima D, Amadou S, Baye DH, Price Polycarpe DB, Bourahima K, Moumine S, Dit Sadio SY, Ousmane K, Bocar B, Mohamed T, Boubakar TA, Sidy B, Mamoudou M, Michael B, Seydou D, Bassirou D, Ibrahima I M, Souleymane D. Performance of Xpert MTB/RIF in comparison with light-emitting diode-fluorescence microscopy and culture for detecting tuberculosis in pulmonary and extrapulmonary specimens in Bamako, Mali. Int J Mycobacteriol 2020;9:397-404

How to cite this URL:
Combo Georges TA, Aissata T, Fatimata D, Abou CC, Gagni C, Moise SA, Boureima D, Amadou S, Baye DH, Price Polycarpe DB, Bourahima K, Moumine S, Dit Sadio SY, Ousmane K, Bocar B, Mohamed T, Boubakar TA, Sidy B, Mamoudou M, Michael B, Seydou D, Bassirou D, Ibrahima I M, Souleymane D. Performance of Xpert MTB/RIF in comparison with light-emitting diode-fluorescence microscopy and culture for detecting tuberculosis in pulmonary and extrapulmonary specimens in Bamako, Mali. Int J Mycobacteriol [serial online] 2020 [cited 2021 Jan 24];9:397-404. Available from: https://www.ijmyco.org/text.asp?2020/9/4/397/303445

  Introduction Top

Tuberculosis (TB) is an infectious disease caused by a bacterium called Mycobacterium tuberculosis complex (MTBC).[1] In 2018, according to the World Health Organization (WHO), an estimated 10 million people (ranking from 9.0 to 11.1 million) were infected with TB worldwide, a figure that has remained constant in recent years (WHO. Global tuberculosis report 2019, ISBN 978-92-4-156571-4, CIP data are available at http://apps.who.int/iris. accessed 30 October 2019). The burden of TB varies greatly from country to another, from <5 to more than 500 new cases per 100,000 people per year, with a global average of about 130 per 100,000 people,[2] and the emergence of multidrug-resistant tuberculosis (MDR-TB) increases this phenomenon.[3] According to the Mali National TB Program and the WHO report, the prevalence and incidence rates of TB were 91 and 55, respectively, for 100,000 habitants; with 6889 new TB cases notified, among which, 125 MDR-TB or chronic-TB patients were reported.[4] While the prevalence and incidence rates are decreasing since 2000 in Mali, there is an increase of drug resistance (DR) within the country, mainly the primary MDR-TB, which moved from 2.5% in 2011 to 3.4% in 2016.[5] The main diagnostic tests for TB are sputum smear microscopy, culture-based methods, and rapid molecular assays. It is vital to assess the role of smear microscopy in the diagnosis of TB, especially with the rapid molecular nucleic acid amplification test (NAAT), Xpert MTB/RIF approved by the WHO.[6] There are a number of rapid and automated nucleic acid amplification techniques that have been expand for the detection and identification of MTBC, including mutations that confer DR in sputum samples from TB patients.[7],[8],[9] However, sputum microscopy assay remains the most commonly used technique for initial diagnostic test of TB in developing countries, where most cases and deaths associated with TB occur.[10] It is a simple, quick, and low-cost technique to quantify and identify highly contagious patients, which is very specific to countries where the prevalence of TB is very high.[10],[11],[12] Nevertheless, the sensitivity of microscopy assay is significantly compromised when the bacillary load is smaller than 10,000 organisms/mL in samples, also in detecting new cases, and HIV/TB coinfection.[13] Over the past years, fluorescence microscopy has demonstrated the potential for increasing the performance of microscopy in the diagnosis of TB and needs to be explored for it efficiency with other existing methods.[14],[15],[16]

Mycobacterium tuberculosis (MTB) culture assay is considered as the reference method for the diagnosis of TB, however, it is a slow process that can take several weeks (up to 8 weeks) and requires appropriate infrastructure and technical skills.[13],[17],[18] The WHO endorsed in 2011 the Xpert® MTB/RIF assay, for the diagnosis of TB,[7] a method with sensitivity and specificity that approaches MTB culture assay.[19],[20] Xpert MTB/RIF uses a real-time polymerase chain reaction (RT-PCR) principle that can detect simultaneously the specific sequence of MTB and that of rifampicin to resistance (RR).[21],[22] The Xpert MTB/RIF test for pulmonary TB is high.[23],[24] However, it is strongly advised that the molecular test be performed and interpreted in the context of the comprehensive testing algorithm that includes smear and culture as well as a first-line drug sensitivity test to increase its benefits for patient management.[20],[25] Thus, in 2011, the WHO policy stated that patients with a high risk of TB, like presumptive HIV-associated TB patients and pediatric presumptive TB, including extrapulmonary cases in whom acid-fast bacilli (AFB) smear examination is usually negative, are the most likely to be benefited from Xpert MTB/RIF.[24],[26] Xpert MTB/RIF was introduced in Mali in 2014 at the national reference laboratory and thereafter in our research and diagnostic institution (SEREFO/University Clinical Research Center [UCRC], Mali) 2 years later. Thus far, there are limited data regarding the performance of Xpert MTB/RIF assay compared to light-emitting diode (LED)-FM considering culture as a reference tool of diagnostic in a high TB incidence setting such as Mali. Thus, this present study seeks to evaluate the specificity, sensitivity, positive predictive value (PPV), and negative predictive value (NPV) of Xpert MTB/RIF and LED-FM methods compared to the MTB culture as a gold standard method.

  Method Top

Study design and setting

A retro-prospective study was conducted by reviewing laboratory-based results of suspected TB patients that was collected from January 2016 to June 2019 and tested with auramine-based sputum LED-FM, Xpert MTB/RIF, and MTB culture methods at the UCRC of the University of Sciences, Techniques and Technologies of Bamako (USTTB), Bamako, Mali. The UCRC Biosafety Laboratory Level 3 is a certified laboratory by the College of American Pathologists, including external quality controls.

Participants' recruitment

We consecutively enrolled adults and children suspected of pulmonary or extrapulmonary TB. Patients were included based on clinical suspicion of TB, including coughing more than 2 weeks with or without expectoration.

Participants were enrolled at the six referral health centers in Bamako, Mali and the department of pneumology at the teaching hospital of Point-G, Bamako, Mali. Throughout that time, all patients with clinically new suspected TB or suspected treatment failure (retreatment) had at least one sample collected and tested with all the three tests (LED-FM, Xpert MTB/RIF, and culture). We excluded participants with missing either auramine-based sputum LED-FM results, Xpert MTB/RIF, and/or culture results. Indeterminate results of Xpert MTB/RIF after two tests were considered as missing data.

Ethical considerations

Patients were enrolled in an institutional review board-approved protocols. Thus, before starting, all protocols were approved by the Ethics Committee of the Faculty of Medicine, Dentistry, and Pharmacy of the USTTB. Consent was obtained from each participant before inclusion in this study. Data were identified and analyzed and presented as aggregate results.

Samples and data collections

Sputum samples were obtained from new pulmonary suspected TB patients based on complaining from cough for more than 2 weeks, and treatment failure's group was defined as smear positive after 5 months of starting anti-TB drugs based on Malian national algorithm. Other specimens were collected from extrapulmonary suspected patients, including pleural liquid, peritoneal effusions, and bronchoalveolar aspirates. Usually, two samples were collected from pulmonary TB patients, while one sample was obtained from the extrapulmonary suspected patients. Patient's demographic data, such as the referral facility, age, and sex, as well as HIV status and the results of LED-FM, were obtained from patients at the enrollment sites. The different tests performed at the UCRC laboratory were documented on the data collection forms.

Laboratory tests

Suspected TB samples (either sputum, urine, superficial swabs, or gastric aspirates) were received in the laboratory from different referral health centers of Bamako, Mali, as per the collection and transportation policies of the laboratory. Xpert MTB/RIF assay was performed using a standard protocol, and liquid culture was executed employing Mycobacterium growth indicator tube assay. Sputum smear microscopy by FM using auramine O staining-based LED-FM (BBL Becton Dickinson, Sparks MD, USA) was initially performed at local health reference centers.

Xpert MTB/RIF method

Xpert MTB/RIF testing was performed, as stated by the manufacturer's instructions.[27] At the same time, it detects both MTBC and the resistance to rifampicin (RR). Briefly, Xpert MTB/RIF is a NAAT in a closed platform, i.e., entirely integrated and automated. It combines sample preparation within the same cartridge as well as real-time PCR (amplification and detection). Moreover, when MTBC is detected, a semi-quantitative scale is provided for each of five probes showing cycle threshold (Ct) worth, which are conversely correlated to the quantity of target DNA in the sample.

Ct values correlate well with smear positivity, and patients with smear-negative pulmonary TB have a higher Ct value.[28] In addition, each probe should bind to the specific wild-type region of the rpoB gene, and the absence of hybridization between a particular probe and its corresponding wild type is suggestive of mutation and thus TB-RR (resistance to rifampicin).

Microscopy, culture, and identification

Sputum or extrapulmonary samples were digested, decontaminated and centrifuged using the N-Acetyl-L-Cysteine/4% NaOH mixture, concentrated by centrifugation (4500 rpm), and inoculated on two media liquid and solid (Middlebrook 7H11 Agar and Selective 7H11 Agar). Concomitantly, keep the sediment in - 80 and prepare indirect staining microscopy. The characterization of the positive mycobacterial cultures was carried out on the presence of bacillus under microscopy as well as the shape of the colony on a solid medium and was confirmed by Capilia TB Test. Cultures were followed two times a week for growth and subsequent identification.

The microscopy gradient of the sputum smear was performed as follows the International Union Against TB and Lung Disease rating criteria as negative (no AFB seen or zero), low AFB seen (1–9 AFB per 100 fields with immersion), very low AFB seen (10–99 AFB seen in 100 fields or 1+), moderate AFB seen (1–10 AFB seen per field or 2+), and high AFB seen (>10 AFB seen per field or 3+).[29],[30],[31] To reduce errors, two specialists evaluated the smears, and in case of discrepancies, another person was designed to analyze them.

Data analysis

Demographic data, including experimental data of the study, were analyzed using Epi Info™ version Contingency tables were used to determine the PPV, NPV, specificity, sensitivity, the 95% confidence interval and the performance of Xpert MTB/RIF. Positive and negative likelihood proportions and the k Cohen coefficient were calculated for LED-FM and Xpert MTB/RIF assays employing MTB culture as a reference method in this work.

By considering culture as a reference method, specimens that were positive and negative in culture assay were suggested as true positive and negative results. Negative culture and Xpert MTB/RIF-positive specimens were recorded as false-positive results. Xpert MTB/RIF-negative and Xpert MTB/RIF-positive culture specimens were inspected false negative. The statistical analysis was considered statistically significant when P < 0.05.

  Results Top

A total of 697 TB-suspected patients who met the inclusion criteria were retrieved from the Data Bank files. Out of the 697 TB patients, 642 (92%) were respiratory TB and 55 (8%) were nonrespiratory TB specimens.[Figure 1]
Figure 1: Study population. Descriptive diagram of the study

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The mean value of age of the study participants was 37.56 years within the range of 14–86 years [Table 1]. The group of age between 14 and 30 years was the most represented in this study (n = 234 [37.80%]). There were more males (n = 493 [70.73%]) than females (n = 204 [29.27%]). HIV status was documented for 452 (64.85%) individuals, among which 82 (11.76%) were positive.
Table 1: Sociodemographic and biological characteristics of the study participants

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Light-emitting diode-fluorescent microscopy

Overall, in this study population, the LED-FM assay resulted in 519 (74.46%) smear positives and 178 (25.54%) smear negatives. Specifically, among pulmonary samples, 496/642 (77.26%) were smear positive, while in extrapulmonary specimens, 23/55 (41.82%) were smear positive.


For Xpert MTB/RIF assay, 509/642 (79.28%) suspected TB patients were positive and 133/642 (20.72%) were negative for sputum samples, while 4/55 (7.27%) extrapulmonary samples were positive for TB.

Mycobacterium tuberculosis culture

Of the 697 samples, 584/697 (83.79%) were culture positive. The culture positivity rate in pulmonary and extrapulmonary patients was 564 (87.85%) and 20 (36.36%), respectively.

Sensitivity, specificity, positive predictive values, and negative predictive values in all population studied

The LED-FM sensitivity rate was lower in general in pulmonary samples (87.8%) compared to extrapulmonary samples (95%). However, its specificity was shown to be higher in pulmonary samples (98.7%) than in extrapulmonary samples (88.6%).

In contrast to LED-FM, Xpert MTB/RIF sensitivity rate was higher in pulmonary than extrapulmonary samples (89.9% vs. 45%), and the specificity of Xpert MTB/RIF was slightly higher in extrapulmonary samples (100.0%) than pulmonary samples (97.4%).

In naÏve treatment patients, the LED-FM test had a sensitivity of 83.9% and a specificity of 100%, while in previously treated patients, the sensitivity and specificity were 94.2% and 0.00%, respectively. In both the groups, the Xpert MTB/RIF test had a sensitivity of 87.1% versus 94.7% and a specificity of 98.7% versus 0.00%, respectively [Table 2].
Table 2: Performance of smear microscope (auramine/rhodamine), Xpert compared to the culture test

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The PPVs were similar in both naÏve and previously treated cases (99.7% vs. 99.5%). The sensitivity and specificity of naÏve and previously treated patients were 83.9% versus 94.2% and 100% versus 0.0%, respectively, and the PPV was 100% versus 57.4% and NPV was 99.5% versus 0.0% for both the groups, respectively [Table 2].

In the general sampling (pulmonary and extrapulmonary samples), the sensitivity was higher in Xpert MTB/RIF than LED FM (99.6% vs. 88.0%), and the specificity was observed to be higher in LED-FM compared to Xpert MTB/RIF (95.6% vs. 62.0%), however, the performance of Xpert remained higher than LED-FM.

The sensitivity of Xpert MTB/RIF and LED-FM was 83.8% versus 100% among HIV-positive and HIV-negative TB patients correspondingly.

  Discussion Top

A comparative study of different available TB diagnostic tools was conducted in order to provide a better option to rapidly and more adequately manage TB infection in developing countries, particularly in Mali. In this study, we compared the performance of Xpert MTB/RIF to LED-FM method for detecting pulmonary and extrapulmonary TB with MTB culture method as a gold standard assay. All methods mentioned except MTB culture were performed as a rapid diagnostic test in individuals with presumptive TB infection.[32] In the study, we observed that the sensitivity, specificity, PPV, and NPV of Xpert MTB/RIF technique for all tested samples were 99.9%, 62.0%, 88.4%, and 98.2%, respectively. These findings possess some similarities with previously reported studies, such as the one conducted by Sharma et al. in order to evaluate the diagnostic accuracy of this method, where they demonstrated that the sensitivity, specificity, PPV, and NPV of Xpert MTB/RIF were 95.7%, 99.6%, 99%, and 98.1%, respectively.[33],[34],[35],[36] The sensitivity, specificity, PPV, and NPV of LED-FM assay for both pulmonary and extrapulmonary samples were found to be 88.0%, 95.6%, 99.0%, and 60.7%, respectively. In pulmonary TB samples, the sensitivity and specificity of LED-FM were 87.8% and 98.7%, respectively, while a study conducted by Cattamanchi et al. demonstrated a sensitivity of 72% and a specificity of 81% employing fluorescent microscopy,[37] another study conducted by Bhadade et al.[16] reported a sensitivity and a specificity of 67.53% and 88.71%, respectively, and also, Bhalla et al.[14] showed a sensitivity of 83.1% and a specificity of 82.4% using LED-FM. This result slightly differs with our current findings; nevertheless, the differences must be due to the sample size and the used of mercury vapor lamp fluorescent microscopy by Cattamanchi et al. However, John Osei Sekyere et al. observed similar sensitivity and specificity (82% and 90.28%, respectively).[38] In extrapulmonary samples, the sensitivity and specificity of LED-FM were 95% and 88.6%, respectively, in contrast to the finding reported by John Osei Sekyere et al. where the sensitivity was 53.85% and the specificity was 98.51%.[38] The Xpert MTB/RIF test demonstrated a sensitivity of 89.9%, whereas the specificity was 97.4% in detecting MTBC in sputum samples; on the other hand, the PPV was 99.6% and the NPV was 57%. Other studies reported similar results such as the findings of Munir et al.,[39] where they showed the performance of Xpert MTB/RIF with a sensitivity of 90.1% and specificity of 98.3% in detecting MTBC. A study by Sudhamani[40] conducted in 2016 also found that the sensitivity and specificity of the Xpert MTB/RIF were 100%, respectively, when compared with culture method. Zeka et al.[41] in 2011 reported an 82.3% sensitivity and a 100% specificity of Xpert MTB/RIF, like Rrezarta Bajrami et al.,[20] in 2018 who reported an 82.3% sensitivity and a 97.6% specificity of Xpert MTB/RIF. Elsewhere, Walusimbi et al.[42] in 2013 showed that the sensitivity was low (48.8%) but with a better specificity (95.1%).

We found that our study is an important addition to the scientific literature, for the reason that it represents one of the largest sample sizes from both respiratory and nonrespiratory specimens tested with Xpert MTB/RIF technique, in the exception of a study carried out in India by Friedrich et al.[43]

The observed sensitivity of Xpert MTB/RIF was 45.0% for extrapulmonary TB, and three other studies reported similar sensitivities ranging from 25.0% to 58.3%.[43],[44],[45] However, the Xpert MTB/RIF sensitivity from our study remained lower when compared to the sensitivity reported by Vadwai et al. with 83%,[46] 94.4% by Al-Ateah et al.,[47] 85.7% by Malbruny et al.,[48] 75% by Zmak and Jankovic,[49] and 82.3% by Bajrami et al.[50] This low sensitivity of Xpert MTB/RIF in the extrapulmonary TB samples observed from the current study may be due to the paucibacillary of the sample, or it is possible that the bacterial load may have been too low for the GeneXpert to detect the genetic elements of MTBC whether other infectious diseases such as HIV might have influenced the sensitivity of Xpert MTB/RIF.

The sensitivity of smear microscopy was 95%, which was higher than other studies reported by Vadwai et al. (51%),[46] Al-Ateah et al. (33.3%),[47] and Malbruny et al. (28.6%).[51] In contrast, our auramine-based staining microscopy method used a concentrated pellet of sample after decontamination and centrifugation procedure. Thus, the concentration step increases the yield of smear positivity.

In HIV-infected individuals, the sensitivity of smear microscopy was observed to be low (11.76%), in contrast to other reported studies, which were ranking from 30% to 48%.[52],[53],[54] Among HIV infected patients, Bhadade et al. in comparison with solid culture as a reference standard found that LED-FM has a sensitivity of 67.53% and a specificity of 88.71% which demonstrates the utility of this technique in the diagnosis of TB-coinfected individuals with HIV.[16] Some limitations were observed in our study, including the retro-prospective approach which may have precluded to firmed conclusion because of the loss of sensitive information. In addition, we have more patients who were not included due to missing data either on smear microscopy or culture results and have used patients who were diagnosed in an urban area of the district of Bamako, Mali, only whom may have different results from rural areas of the country, Mali. Despite these limitations, we studied a relatively high sample size to validate Xpert MTB/RIF in both respiratory and extrapulmonary samples. In addition, given that almost all the regions in Mali have an Xpert MTB/RIF machine and auramine-based LED-FM, thus, a wide sample size of samples from all regions of Mali would be essential for obtaining a right country profile of Xpert MTB/RIF performance. Thus far, multidrug susceptibility testing (phenotypic) will remain only available in the capital city, Bamako at the reference laboratory (SEREFO-UCRC Laboratory). The countrywide oversight of TB treatment failure would benefit from lager performance of the GeneXpert MTB/RIF assay by providing accurate continuous surveillance results on nationwide DR rates.

  Conclusion Top

Xpert MTB/RIF and auramine O staining-based LED-FM share almost the same sensitivity (89.9% vs. 87.8%) and specificity (97.4% vs. 98.7%) in pulmonary samples, while in extrapulmonary samples, Xpert MTB/RIF sensitivity (45%) was lower compared to LED-FM assay (95%). However, the performance of Xpert MTB/RIF was higher than of the LED-FM assay in all the samples (99.6% vs. 88%). Therefore, Xpert MTB/RIF can be a helpful diagnostic tool for individuals with presumptive pulmonary TB as well as for extrapulmonary TB due to its sensitivity and specificity in rapidly and simultaneous detecting MTBC and rifampicin resistance profile which is particularly advantageous inpatient management with MDR-TB and HIV-associated TB.

Suspected TB samples with positive Xpert MTB/RIF results but negative for MTB cultures need to be interpreted with caution and should be consistent with clinical and treatment history of the patient. This study showed that Xpert MTB/RIF-based approach in diagnosing TB either in pulmonary or extrapulmonary specimens is much effective than smear microscopy methods.


We acknowledge the Diagnostics of MDR-TB in Africa project and the European and Developing Countries Clinical Trials Partnership for supporting this study.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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  [Table 1], [Table 2]


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