P a g e | 2710 J. Med. Pharm. Chem. Res. 7 (2025) 2710-2717
FULL PAPER
Comparison of diagnostic value between lipoarabinomannan test and gene xpert MTB/RIF ultra for diagnosis of pulmonary tuberculosis in urine HIV patients
Chiquita Hasri Mirandaria |Aryati Aryatib,* |Dwi Rahayuningsihb |Musofa Ruslic
Introduction
Human Immunodeficiency Virus (HIV) is an infection that attacks the immune system,
especially CD4 cells, and it cause of high mortality in the world. The World Health Organization (WHO) in 2022 reported that 39 million people were living with HIV and
aClinical Pathology Specialization Program, Departement of Clinical Pathology, Faculty of Medicine, Universitas Airlangga, Surabaya, Indonesia
bDepartement of Clinical Pathology, Faculty of Medicine, Universitas Airlangga, Surabaya, Indonesia
cDepartement of Internal Medicine, Faculty of Medicine, Universitas Airlangga, Surabaya, Indonesia
*Corresponding Author:
Aryati Aryati
Tel.: +6281230570493
HIV is an infection that attacks the immune system, especially CD4 cells, making them more susceptible to infections, such as tuberculosis (TB). Some laboratory examination methods used to diagnose pulmonary tuberculosis such as microscopic examination, Polymerase-Chain-Reaction (PCR), and culture. All of these methods use sputum samples while suspected pulmonary TB HIV-AIDS patient have difficulty producing good sputum, so other samples such as urine are needed as an alternative. This study aims to compare the diagnostic value of urine lipoarabinomannan test and GeneXpert MTB/RIF Ultra urine to diagnose of pulmonary tuberculosis in HIV patients. This cross-sectional study is using urine specimens from HIV patients with pulmonary TB and without pulmonary TB at Dr. Soetomo General Hospital in May-September 2024. Urine lipoarabinomannan test and GeneXpert MTB/Rif Ultra urine were performed at Clinical Pathology Laboratory. Diagnostic values and Kappa index were analysed using SPSS 24.0 software.
The diagnostic value of urine lipoarabinomannan test is better than urine GeneXpert MTB/Rif Ultra, with (67% sensitivity; 95%
specificity vs. 26.19% sensitivity; 100% specificity). The suitability analysis of the urine lipoarabinomannan test with the sputum GeneXpert MTB/RIF for diagnosing pulmonary tuberculosis in HIV patients showed better results than the urine GeneXpert MTB/RIF Ultra. Urinary lipoarabinomannan testing has increasing diagnostic value in CD4 <200 cells/mm3 HIV patients. The diagnostic value analysis of the urine lipoarabinomannan test is better than GeneXpert MTB/RIF Ultra urine. Therefore, it can be used as an additional diagnostic tool for diagnosing pulmonary TB, especially for HIV patients.
KEYWORDS
Urine lipoarabinomannan testing; GeneXpert MTB/RIF Ultra urine; Pulmonary TB; HIV.
630,000 mortalities. This weakened immune system makes someone with HIV more susceptible to infections, such as tuberculosis (TB) [1]. The estimated national TB cases in 2021 were 969,000, with findings of HIV cases with TB of 22,000 cases. The mortality rate estimated at 2.4 per 100,000 population [2].
Several laboratory examination methods used to establish tuberculosis include microscopic BTA examination, Polymerase Chain Reaction (PCR), culture, and Interferon- Gamma Release Assay (IGRA), but most of that use sputum samples and invasive, while according to Shapiro 2022, the use of sputum samples in TB diagnostic examinations has many obstacles for people with HIV, such as difficulty in producing good quality sputum due to a weakened body, so other non-invasive samples such as urine are needed as an alternative for TB diagnostic confirmation [3].
The WHO 2019 has recommended a point- of-care test (POCT) tool use urine sample that can detect Mycobacterial Lipoarabinomannan (LAM) to help confirm the diagnosis of tuberculosis in HIV-positive patients [4]. This is also recommended by the Indonesian Ministry of Health in 2023 [5]. The tool uses an immunochromatography method so that it can detect LAM antigens quickly. Tuberculosis examination that can use urine samples other than TB-LAM is GeneXpert MTB/RIF Ultra. The Indonesian Ministry of Health in 2020 has released technical instructions for TB examination with non-sputum body fluid specimens, such as CSF, tissue, and others other than blood, but the diagnostic capability of GeneXpert MTB/RIF Ultra with urine samples for establishing pulmonary TB has not been officially reported, so the aims to this study was to find the comparison of the diagnostic value of the urine lipoarabinomannan test and GeneXpert MTB/RIF Ultra to help establish the diagnosis of pulmonary tuberculosis in HIV patients.
Materials and methods Sample
This cross-sectional study has 82 samples. The sample size was calculated using sample size formula in prevalence study [6]. The prevalence for sample size calculation was estimated from Zeru study in 2021, which showed the prevalence of pulmonary TB and HIV was 37.4% [7]. All samples were collected from May 2024 to September 2024 from inpatient and outpatient clinic of Dr. Soetomo General Hospital. The samples were divided into 2 groups. The first group consisted of 42 samples HIV with pulmonary TB and the second group consisted of 40 HIV groups without pulmonary TB samples. The urine samples used suitable for the inclusion and exclusion criteria. The inclusion criteria included age >18 years, men and women who had been diagnosed with HIV regardless of CD4 levels, female patients that did not on menstruation, normal urine specific gravity (1.003-1.030), and were willing to participate in the study by signing an informed consent.
The HIV group with pulmonary TB is an HIV patient who has been diagnosed with pulmonary TB based on anamnesis, clinical examination, and radiology, accompanied by positive GeneXpert MTB/RIF sputum results.
The HIV non-pulmonary TB group is an asymptomatic pulmonary TB HIV patient either from anamnesis, physical examination, and/or radiology, and the diagnosis of non- pulmonary TB has been confirmed by an internist who is a consultant for tropical infectious diseases, as well as HIV patients with non-specific symptoms of TB but negative GeneXpert MTB/RIF results. Exclusion criteria are HIV patients with a diagnosis of extrapulmonary TB that has been confirmed by a clinician. Patients in both groups also had red blood samples for CD4 examination.
Ethics
This study first received approval from the Health Research Ethics Committee of Dr.
Soetomo Regional General Hospital.
Examination procedure
1) Urine samples according to inclusion and exclusion criteria were collected in a urine tube, analysed less than an hour, and then performed FujiLAM (Fujifilm, Japan) for TB- LAM and GeneXpert MTB/RIF Ultra urine (Cepheid, USA). Urine samples were transferred as much as 200 µL or up to the limit to the aliquot containing the reagent using a pipette. Close the aliquot with a nozzle. After incubating for 40 minutes, 1 drop sample was dripped into the sample port then pressed the '2' mark, if an orange marker appears on 'Go Next' box, pressed the ‘3’ mark. The positive result showed 2 lines on C (Control) and T (Test). If there was only 1 result line on C without the T line so the result was negative.
The examination results are recorded on the sheet provided.
2) Procedure for GeneXpert MTB/RIF Ultra:
Urine sample was transferred to a collection tube, and then the reagent from GeneXpert was added in a 1:1 ratio to urine. The tube was shaken using a vortex 30 seconds for homogenization and incubated for 15 minutes at 20-30 °C, after that sample was inserted into a cartridge around 3 ml or reaching the limit line on the pipette. The GeneXpert MTB/RIF Ultra tool was prepared by entering the cartridge barcode and patient identity. The cartridge was inserted into the rack that displays a green indicator. The tool will process the sample in <80 minutes. The results of the examination are recorded on the sheet provided.
Statistical analysis
All statistical analysis was performed with Statistical Package for the Social Sciences software version 24.0. Diagnostic values
consisted of sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), positive likelihood ratio (pLR), negative likelihood ratio (nLR), and accuracy.
The sensitivity of the test was calculated as (true positive, TP)/(TP + false negative (FN)), and the specificity was calculated as (true negative (TN))/(TN + false positive (FP)). PPV was calculated as TP/(TP+FP), and NPV was calculated as TN/(TN+FN). The positive likelihood ratio (pLR) was calculated as sensitivity/(1–specificity), and the negative likelihood ratio (nLR) was calculated as (1–
sensitivity)/specificity. The PPV was calculated as TP/(TP + FP) and the NPV was calculated as TN/(TN + FN). Accuracy was calculated as (TN + TP)/(TP + FP + FN + TN).
Cohen’s kappa coefficient test was used to assess the level of agreement between TB-LAM and GeneXpert MTB/RIF Ultra. We also measured the sensitivity and specificity of TB- LAM and GeneXpert MTB/RIF Ultra according to CD4 level.
Results
The participants in this study were mostly men (69.05%) than female (30.95%), with the most age between 31-40 years (40.24%). There were 28 patients (67%) had CD4 <200 cell/mm3 in first group and 17 patients (42,5%) had CD4 200-349 cell/mm3 in second group. The results of the examination and comparison of the diagnostic values of the urine lipoarabinomannan test and the GeneXpert MTB/RIF Ultra urine are indicated in (Tables 1 and 2).
Analysis of the urine TB-LAM based on the HIV with pulmonary TB group obtained 67%
(28/42) TP results and 33% (24/42) FN, based on the HIV without pulmonary TB group obtained 95% (38/40) TN and 5% (2/40) FP, while the results of the GeneXpert MTB/RIF Ultra urine examination in HIV with pulmonary TB group obtained 26.19% (11/42) TP results of and 73.81% (31/42) FN, based on
the HIV without pulmonary TB group obtained 100% (40/40) TN and there was no FP.
TABLE 1 Result of TB-LAM and GeneXpert MTB/RIF Ultra
n=82 %
1. Lipoarabinomannan Urine (TB-LAM) HIV with Pulmonary TB:
Positive Negative
n = 42 28
14 67%
33%
HIV without Pulmonary TB:
Positive Negative
n = 40 2
38 5%
2. GeneXpert MTB/RIF Ultra urine 95%
HIV with Pulmonary TB:
Positive Negative
HIV without Pulmonary TB:
Positive Negative
n = 42 11 31 n = 40
0 40
26.19%
73.81%
0%
100%
TABLE 2 Comparison of diagnostic values
Diagnostic Values TB-LAM Urine
(95% CI) GeneXpert MTB/RIF Ultra Urine (95% CI)
Sensitivity 67% (52.41-80.92%) 26.19% (13.86-42.04%)
Specificity 95% (88.24-100%) 100% (91.19-100%)
PPV 93.33% (84.4-100%) 100% (71.51-100%)
NPV 73.08% (61.02-85.13%) 56,34%
pLR 13.34 (3.39-52.34) ~
nLR 0.35 (0.22-0.54) 0.74 (0.62-0.88)
Accuracy 80% (70.4-91.1%) 62.19% (50.99-72%)
Kappa index 0.612 0.257
P <0.001 <0.001
PPV: positive predictive value, NPV: negative predictive value, pLR: positive likelihood ratio, and nLR:
negative likelihood ratio.
The diagnostic value analysis of TB-LAM showed had better sensitivity (67% vs.
26.19%) than GeneXpert MTB/RIF Ultra, but had lower spesificity (95% vs 100%). PPV and NPV of TB-LAM showed 93.33% and 73.08%, with pLR and nLR was 13.34 and 0.35, and the diagnostic accuracy was 80%. The PPV and
NPV of GenXpert MTB/RIF Ultra urine showed 100% and 56.34%. pLR could not be defined, nLR 0.74, and diagnostic accuracy was 62.19%.
The Kappa index of TBLAM showed better agreement (0.612; p<0.001) than GeneXpert MTB/RIF Ultra urine (0.257; p<0.001).
TABLE 3 The diagnostic value TB-LAM and GeneXpert MTB/RIF Ultra urine based on CD4
TB-LAM GeneXpert MTB/RIF Ultra Urine CD4 (cell/mm3) Sensitivity
(95% CI) Specificity
(95% CI) Sensitivity
(95% CI) Specificity (95% CI)
CD4 <200 86%
(72,7-98,6%) 82%
(59-100%) 39%
(21,5-59,4%) 100%
(71,5-100%)
CD4 200-349 33%
(9,9-65,1%) 100%
(80,5-100%) - -
CD4 350-499 - - - -
CD4 ≥500 - - - -
The diagnostic value of the lipoarabinomannan and GeneXpert MTB/RIF
Ultra urine tests based on CD4 is described in Table 3. Analysis of diagnostic value in Table 3
indicates that TB-LAM had better sensitivity than GeneXpert MTB/RIF Ultra urine (86% vs 39%) in HIV patient with CD4 <200 cells/mm3. TB-LAM also had better sensitivity when compared to the overall diagnostic value (86%
vs 67%).
Discussion
The WHO 2019 had recommendation of TB- LAM urine examination in tuberculosis patients with HIV, the elderly, and children [8].
Analysis of diagnostic value TB-LAM using FujiLAM in this study had better sensitivity (67% vs. 64% and 60%) and specificity (95%
vs. 83.3% and 87%) than previous studies [9,10]. Differences in diagnostic values of each study can caused previous study used a large number of research samples, it can be also caused by stability of the analyte, so the samples must be examined immediately without going through a storage process [11].
The samples collected were 28 patients (67%) underwent intensive phase pulmonary TB treatment and 14 other patients (33%) undergoing advanced phase treatment, where according to previous study, showed that intensive phase treatment aims to kill active TB bacteria using a combination of strong drugs, including rifampicin, isoniazid, pyrazinamide, and ethambutol, when many bacteria are destroyed, the bacterial cell wall breaks, releasing more lipoarabinomannan structures, so that tests targeting lipoarabinomannan antigens show positive results, while in advanced phase treatment the bacterial load was reduced, so the LAM antigen is not enough to produce a positive result [4,12].
Accordingly, the used of lipoarabinomannan test better in early stages of diagnosis (before therapy) or when receiving intensive phase therapy, and monitoring antituberculosis treatment in HIV patients. Urinary lipoarabinomannan testing can also be used as an additional diagnostic tool for establishing cases of pulmonary TB in HIV.
This study has 2 positive results in lipoarabinomannan examination, it can occur due to cross-reactions with non-tuberculous mycobacterial infections or bacterial or fungal contamination in urine specimens [13]. The lipoarabinomannan structure that can be detected in this examination is also possessed by bacteria other than Mycobacterium tuberculosis, including Mycobacterium smegmatis and Corynebacterium glutamicum, so it can cause FP results [14].
The WHO has recommendation for replacement of GeneXpert MTB/RIF with Ultra for established TB using nested Real-Time Polymerase Chain Reaction (RT-PCR) method since March 2017 [15]. The diagnostic value analysis of GeneXpert MTB/RIF Ultra urine in this study showed a low sensitivity with high specificity (26.19% and 100%, respectively).
However, this study had higher value of sensitivity and specificity compared to previous study (17.2% and 98.1%, respectively) [16].
The positive result of this study was only 11 of 42 in the first group. The low positive rate can be caused by several things, including the absence of a standard procedure for handling urine samples by Cepheid, and there were different procedures from previous journals that support this study. It can also cause the several tests used to detect MTB DNA in urine, such as Xpert MTB/RIF Ultra (Cepheid, Sunnyville CA), were not designed to pick up small DNA fragments that may be present in urine or known as transrenal DNA, while the target primers owned by GeneXpert MTB/RIF Ultra was IS1081/IS6110 and rpoB 1-4 [17,18]. Transrenal DNA (trDNA) of Mycobacterium tuberculosis (MTB) is a DNA fragment originating from TB bacteria that has been filtered and cleaned through the kidneys after being broken down by the body's system.
When TB bacteria spread in the body, some of its DNA fragments can pass through the kidney membrane and exit through urine in the form of small fragments called transrenal DNA [17].
The diagnostic value analysis of the urine lipoarabinomannan test showed better results (sensitivity 86%, specificity 82%) compared to GeneXpert MTB/RIF Ultra urine (sensitivity 39%; specificity 100%) in HIV patients with CD
<200 cells/mm3. The diagnostic value was also higher when compared to the overall urine lipoarabinomannan test (sensitivity 67%, specificity 95%). This results also the same as previous studies which showed of increasing sensitivity [10,19]. The increase in sensitivity can be caused by the increasing number of true positives in the first group. A decreasing CD4 count indicates weak immunological status, making it more difficult for the body to control Mycobacterium tuberculosis (MTB), make an increasing of bacterial load in the patient’s body. This makes the LAM structure easily captured by high-avidity monoclonal antibodies that contained in TB-LAM [4]. The limitations of the study reveal that this study did not stratify according to TB treatment phase and viral load. Likewise, this study did not perform sputum and urine examination in the same time.
Conclusion
The diagnostic analysis of the urine lipoarabinomannan test (sensitivity 67%, specificity 95%) showed better results when compared to GeneXpert MTB/RIF Ultra urine (sensitivity 26.19%, specificity 100%) for diagnosing pulmonary tuberculosis in HIV patients. The urine lipoarabinomannan test also has a higher diagnostic value (sensitivity 86%, specificity 82%) compared to GeneXpert MTB/RIF Ultra urine (sensitivity 39%;
specificity 100%) in HIV patients with CD <200 cells/mm3. Accordingly, the urine lipoarabinomannan test can be used as an additional diagnostic tool for diagnosing pulmonary TB cases in HIV patient, and GeneXpert MTB/RIF Ultra with urine samples still cannot replace sputum-based diagnostic tools.
Lipoarabinomannan test also has better possibility if used in the early phase of diagnosis (before therapy) or when receiving intensive phase therapy, as well as monitoring antituberculosis treatment in HIV patients.
Suggestions for further research considerations using MTB culture as the gold standard, and using standardized procedures from Cepheid for GeneXpert MTB/RIF Ultra with urine samples, it can use another urinary lipoarabinomannan tests as a comparison, and research in the pediatric population.
Acknowledgments
We want to thank the Dean of the Faculty of Medicine, Airlangga University, and the Director of Dr. Soetomo General Hospital.
Ethical issues
The study was approved by the Committee of Research and Ethics in Dr. Soetomo General Hospital (Surabaya, Indonesia). Written informed consent of individual participants was collected. All participants signed to give their approval.
Funding
This study was sponsored by Fujifilm Corporation, Tokyo, Japan. However, all authors were objective with the result without interference of the sponsors.
Authors' Contributions
All authors have made significant contribution in the study.
Conflict of Interest
The authors in this study stated there was no conflict of interest. Authors’ contributions: All authors have made significant contribution in the study.
Orcid:
Chiquita Hasri Mirandari:
https://orcid.org/0009-0004-9593-5796 Aryati Aryati*:
https://orcid.org/0000-0002-9383-6354 Dwi Rahayuningsih:
https://orcid.org/0009-0008-7207-470X Musofa Rusli:
https://orcid.org/0000-0002-4834-2259
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How to cite this article: Chiquita Hasri Mirandari, Aryati, Dwi Rahayuningsih, Musofa Rusli, Comparison of diagnostic value between lipoarabinomannan test and gene xpert MTB/RIF ultra for diagnosis of pulmonary tuberculosis in urine HIV patients. Journal of Medicinal and Pharmaceutical Chemistry Research, 2025,
7(12), 2710-2717. Link:
https://jmpcr.samipubco.com/article_2181 48.html
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