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Original Article

Chest X‑ray Findings Comparison between Multi‑drug‑resistant


Tuberculosis and Drug‑sensitive Tuberculosis
Aziza Ghanie Icksan, Martin Raja Sonang Napitupulu, Mohamad Arifin Nawas1, Fariz Nurwidya1
Department of Radiology, Persahabatan Hospital, 1Department of Pulmonology and Respiratory Medicine, Persahabatan Hospital, Faculty of Medicine, Universitas
Indonesia, Jakarta, Indonesia

Abstract
Background: Imaging has a big role in tuberculosis (TB) diagnosis and chest X‑ray is preferable because it is available in primary health
care and can point out the location, area, and morphology of lesions, such as cavity, consolidation, pleural effusions, and fibrosis. We aimed
to compare the chest X‑ray findings in multi‑drug resistant TB (MDR‑TB) and in drug‑sensitive TB (DS‑TB) cases. Methods: This is a
retrospective cross‑sectional study which compares chest X‑ray findings of two groups of patients, involving 183 DS‑TB patients and 183
MDR‑TB patients. Radiologic findings that we analyzed were infiltrate, consolidation, cavity, ground glass opacity, fibrosis, bronchiectasis,
calcification, node, atelectasis, bullae, emphysema, and other nonlung parenchymal findings. Results: MDR‑TB group have 177 (96%) patients
with large lesions, 6 (4%) with medium lesions, and no small lesions. DS‑TB group have 55 (30%) patients with small lesions, 78 (43%) with
medium lesions, and 50 (27%) with large lesions. Active TB lesions in the forms of infiltrate and ground‑glass opacity were more dominant
in DS‑TB group, whereas consolidation, cavity, fibrosis, bronchiectasis, calcification, node, atelectasis, bullae, emphysema, and other nonlung
parenchymal findings, were more dominant in MDR‑TB. Conclusions: There were significant differences in chest X‑ray findings between
MDR‑TB and DS‑TB in terms of lesion size and morphology. Recognition of chest X‑ray findings could help the physician to differentiate
patient with suspected MDR‑TB.

Keywords: Chest X‑ray, drug‑sensitive tuberculosis, multi‑drug resistant tuberculosis

Introduction X‑ray. Chest X‑ray is preferable because it is available in


primary health care and can point out the location, area, and
Tuberculosis (TB) is a chronic granulomatous disease
morphology of lesions, such as cavity, consolidation, pleural
caused by Mycobacterium tuberculosis (MTB) that has been
effusions, and fibrosis.[3,4] These findings are very important
announced as a global health emergency by the World Health
considering the increasing number of MDR‑TB cases, either
Organization (WHO). TB has infected approximately a third
new or old ones because chest X‑ray evaluates the response
of world population with estimated 1.6 million mortality
of the therapy so that early diagnosis of MDR‑TB can be
yearly.[1‑3] Among those infected, 3.5% of new cases and
achieved.[2,5,6]
20.5% of old cases are infected with multi‑drug resistant
TB (MDR‑TB).[4,5] Indonesia is the 8th country with the most To have a better early diagnosis for TB, a basic knowledge to
MDR‑TB cases in the world, with estimated 6900 cases or differentiate chest X‑ray findings between drug‑sensitive TB
1.9% from new cases and 12.5% of old cases.[1,5] MDR‑TB (DS‑TB) and MDR‑TB are needed.[2,5,6] Until now, there are
diagnosis is made by performing the drug‑sensitivity test of
MTB and supported by physical examination, microbiology, Address for correspondence: Dr. Fariz Nurwidya,
and radiology. Department of Pulmonology and Respiratory Medicine, Faculty of Medicine,
Universitas Indonesia, Persahabatan Hospital, Jalan Persahabatan
Imaging has a big role in TB diagnosis due to the limitations Raya No. 1, Rawamangun, Jakarta 13230, Indonesia.
of microbiology examinations in Indonesia. Radiologic E‑mail: [email protected]
examinations that can be used to diagnose TB and evaluate
therapy in Indonesia are computed tomography and chest
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Access this article online and build upon the work non-commercially, as long as the author is credited and the new
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Website: For reprints contact: [email protected]
www.jnsbm.org

How to cite this article: Icksan AG, Napitupulu MR, Nawas MA,
DOI: Nurwidya F. Chest X‑ray findings comparison between multi‑drug‑resistant
10.4103/jnsbm.JNSBM_79_17 tuberculosis and drug‑sensitive tuberculosis. J Nat Sc Biol Med
2018;9:42-46.

42 © 2018 Journal of Natural Science, Biology and Medicine | Published by Wolters Kluwer - Medknow
Icksan, et al.: MDR and DS‑TB X‑ray findings comparison

not many studies that elaborate the comparison of chest X‑ray


Table 1: Demographic characteristic between multi‑drug
findings in MDR‑TB and DS‑TB cases.
resistant tuberculosis and drug‑sensitive tuberculosis
groups
Methods Characteristic Group P
This study is carried out retrospectively with a comparative
MDR TB (%) DS TB (%)
cross‑sectional study design that compares two groups of patients,
Gender
one with DS‑TB and the other with MDR‑TB. This study
Male 96 (52) 127 (69) 0.001
was conducted in the Department of Radiology, Persahabatan
Female 87 (48) 56 (31)
Hospital, Jakarta, using secondary data that were acquired from Age
the medical record of patients from January 2013 to December <30 35 (19) 49 (27) 0.003
2015. The study protocol was approved by the Ethical Committee 30-39 55 (30) 38 (21)
of Persahabatan Hospital, Jakarta, Indonesia (Ethical Clearance 40-49 56 (31) 42 (23)
Number: 74/KEPK‑RSP/I/2016). A total of patients in this study 50-59 29 (16) 29 (16)
was 183 MDR‑TB patients (96 men and 87 women; mean 39.87 >59 8 (4) 25 (13)
and median age 56 years) and 183 DS‑TB patients (127 men and Mean±SD 39.87±11.59 41.03±12.82
56 women; mean 41.03 and median age 42 years). TB diagnosis MDR: Multi‑drug resistant, TB: Tuberculosis, DS: Drug‑sensitive,
is confirmed from the chest X‑ray results, sputum smear, and SD: Standard deviation
culture results from the medical record.
Active TB lesions, infiltrate in this case, were more dominant
Chest X‑ray results that were obtained from the medical in DS‑TB group compared to MDR‑TB, especially the ones in
record was re‑evaluated by one radiologist who specializes the upper right lung. Consolidation finding is more dominant
in thoracic radiologist and one senior radiology resident. in MDR‑TB in both lungs and can be found in more than one
Assessment of the chest X‑ray results is performed according part of each lung. Consolidation was founded most at the upper
to thoracic assessment form. Chest X‑ray characteristics that left lung (57.4%), middle left lung (55.7%), and upper left
were assessed were 14 types of morphology lesions, area, lung (57.4%). In DS‑TB, 20.8% was found in the upper right
and location of the lesion (s). The obtained data were edited lung, 15.3% middle left lung, and 16.9% in the upper left lung.
and coded, then goes through validation. After validation,
the data were tabulated and calculated using IBM SPSS Consolidations at both lungs in MDR‑TB group were more
Statistics for Windows, Version 20.0. (Armonk, NY: IBM dominant compared to DS‑TB group. These consolidation
Corp). For quantitative data, mean, standard deviation, and findings can be found in more than one part of the lung, either
95% confidence interval were calculated. right or left lung. Most MDR‑TB consolidations were found
in the upper right lung (57.4%), middle left lung (55.7%), and
upper left lung (53%). In DS‑TB group, most consolidations
Results were also found in the upper right lung (20.8%), middle left
Participants and patients lung (15.3%), and upper left lung (16.9%).
The sample for this research was gathered from the medical
Most other radiologic findings, such as cavity, fibrosis,
records of MDR‑TB and DS‑TB patients from Persahabatan
bronchiectasis, calcification, node, atelectasis, bullae,
Hospital, Jakarta. Using this collecting method, 183 patients
emphysema, and other nonlung parenchymal findings, were
from MDR‑TB group and 183 patients from DS‑TB group were
found more in MDR‑TB group. The only exception was ground
gathered and analyzed statistically. Genders of the patients
glass opacity that was found more in DS‑TB group. The details
were mostly male (54% for MDR‑TB and 69% for DS‑TB).
of radiologic findings are shown in Table 2.
Age distributions were mostly 40–49‑year‑old in MDR‑TB
and DS‑TB (31% and 23%, respectively). The mean age was
39.87‑year‑old with 11.59 standard deviation for MDR‑TB Discussion
and 41.03‑year‑old with 12.82 standard deviations for DS‑TB. This study shows the comparison of chest X‑ray findings of
Details for demographic distributions are presented in Table 1. MDR‑TB and DS‑TB in adult patients with the competent
immune system. The population of the MDR‑TB and DS‑TB
Radiologic findings
samples that were recorded in Persahabatan Hospital from
The MDR‑TB group has 177 (96%) patients with large lesions,
January 2013 to December 2015 were 230 and 240 samples,
6 (4%) with medium lesions, and no small lesions. DS‑TB
respectively, and only 183 samples from each group that fulfills
group have 55 (30%) patients with small lesions, 78 (43%) with
the inclusion criteria. Some of the samples are also excluded due
medium lesions, and 50 (27%) with large lesions. Radiologic
to some of the data, such as chest X‑ray, laboratory examination,
findings that we analyzed were infiltration, consolidation,
and drug resistance, are incomplete in the medical record.[3,4]
cavity, ground glass opacity, fibrosis, bronchiectasis,
calcification, node, atelectasis, bullae, emphysema, and other Demographic characteristic distribution of gender in both
nonlung parenchymal findings. groups showed that there are more male than female, 52% male

Journal of Natural Science, Biology and Medicine ¦ Volume 9 ¦ Issue 1 ¦ January-June 2018 43
Icksan, et al.: MDR and DS‑TB X‑ray findings comparison

Table 2: Radiologic finding between multi‑drug resistant Table 2: Contd...


tuberculosis and drug‑sensitive tuberculosis groups Radiologic findings Group P
Radiologic findings Group P MDR TB (%) DS TB (%)
MDR TB (%) DS TB (%) Upper left lung 15 (8.2) 0 0.000
Area of lesion Middle right lung 8 (4.4) 1 (0.5) 0.016
Small 0 55 (30) Middle left lung 11 (6) 0 0.001
Medium 6 (4) 78 (43) Lower right lung 3 (1.6) 0 0.082
Large 177 (96) 50 (27) Lower left lung 4 (2.2) 0 0.044
Infiltrate Node
Upper right lung 67 (36.6) 122 (66.7) 0.000 Upper right lung 10 (5.5) 11 (6) 0.822
Upper left lung 42 (23) 100 (54.6) 0.000 Upper left lung 8 (4.4) 4 (2.2) 0.240
Middle right lung 49 (26.8) 76 (41.5) 0.003 Middle right lung 10 (5.5) 4 (2.2) 0.102
Middle left lung 45 (24.6) 70 (38.3) 0.005 Middle left lung 11 (6) 3 (1.6) 0.029
Lower right lung 22 (12) 49 (26.8) 0.000 Lower right lung 3 (1.6) 2 (1.1) 0.652
Lower left lung 17 (9.3) 52 (28.4) 0.000 Lower left lung 8 (4.4) 0 0.004
Consolidation 1-2 cm nodes 19 (10.4) 13 (7.1) 0.104
Upper right lung 105 (57.4) 38 (20.8) 0.000 2-3 nodes 0 0 0.000
Upper left lung 97 (53) 31 (16.9) 0.000 Solitary node 10 (5.5) 3 (1.6) 0.202
Middle right lung 87 (47.5) 28 (15.3) 0.000 Multiple nodes 9 (4.9) 10 (5.5) 0.734
Middle left lung 102 (55.7) 28 (15.3) 0.000 Atelectasis
Lower right lung 38 (20.8) 18 (9.8) 0.004 Upper right lung 3 (1.6) 7 (3.8) 0.200
Lower left lung 45 (24.6) 12 (6.6) 0.000 Upper left lung 3 (1.6) 0 0.082
Cavity Middle right lung 1 (0.5) 1 (0.5) 1.000
Upper right lung 106 (57.9) 11 (6) 0.000 Middle left lung 1 (0.5) 6 (3.3) 0.056
Upper left lung 89 (48.6) 12 (6.6) 0.000 Lower right lung 1 (0.5) 0 0.317
Middle right lung 71 (38.8) 12 (6.6) 0.000 Lower left lung 1 (0.5) 0 0.317
Middle left lung 95 (51.9) 9 (4.9) 0.000 Bullae
Lower right lung 13 (7.1) 5 (2.7) 0.035 Upper right lung 4 (2.2) 2 (1.1) 0.410
Lower left lung 17 (9.3) 6 (3.3) 0.018 Upper left lung 5 (2.7) 0 0.024
Cavity ≤4 cm 121 (66.1) 26 (14.2) 0.000 Middle right lung 4 (2.2) 1 (0.5) 0.177
Cavity >4 cm 26 (14.2) 3 (1.6) 0.000 Middle left lung 2 (1.1) 0 0.156
Solitary cavity 10 (5.5) 3 (1.6) 0.048 Lower right lung 2 (1.1) 1 (0.5) 0.562
Multiple cavity 125 (68.3) 26 (14.2) 0.000 Lower left lung 1 (0.5) 0 0.317
Ground glass opacity Hyper‑aeration
Upper right lung 2 (1.1) 5 (2.7) 0.252 Upper right lung 0 0 ‑
Upper left lung 1 (0.5) 1 (0.5) 1.000 Upper left lung 1 (0.5) 0 0.317
Middle right lung 1 (0.5) 3 (1.6) 0.315 Middle right lung 0 0 ‑
Middle left lung 2 (1.1) 2 (1.1) 1.000 Middle left lung 1 (0.5) 0 0.317
Lower right lung 1 (0.5) 1 (0.5) 1.000 Lower right lung 1 (0.5) 0 0.317
Lower left lung 0 1 (0.5) 0.317 Lower left lung 2 (1.1) 0 0.156
Fibrosis Nonlung parenchymal
Upper right lung 42 (23) 27 (14.8) 0.045 Right trachea deviation 23 (12.6) 6 (3.3) 0.001
Upper left lung 20 (10.9) 24 (13.1) 0.052 Left trachea deviation 32 (17.5) 6 (3.3) 0.000
Middle right lung 14 (7.7) 13 (7.1) 0.842 Right hilar elevation 35 (19.1) 4 (2.2) 0.000
Middle left lung 13 (7.1) 15 (8.2) 0.694 Left hilar elevation 29 (15.8) 3 (1.6) 0.000
Lower right lung 0 7 (3.8) 0.008 Right pleural effusion 14 (7.7) 3 (1.6) 0.006
Lower left lung 2 (1.1) 12 (6.6) 0.006 Left pleural effusion 36 (19.7) 4 (2.2) 0.000
Bronchiectasis Right thickening 23 (12.6) 1 (0.5) 0.000
Upper right lung 7 (3.8) 10 (5.5) 0.456 Left thickening 18 (9.8) 0 0.000
Upper left lung 6 (3.3) 4 (2.2) 0.521 MDR: Multi‑drug resistant, TB: Tuberculosis, DS: Drug‑sensitive
Middle right lung 25 (13.7) 6 (3.3) 0.000
Middle left lung 17 (9.3) 8 (4.4) 0.062 compared to 48% female in MDR‑TB and 69% male to 31%
Lower right lung 17 (9.3) 9 (4.9) 0.104 female in DS‑TB group. Yoon et al. also had similar findings
Lower left lung 9 (4.9) 3 (1.6) 0.078 and concluded that male is more likely to be infected due to the
Calcification higher exposure and having a higher risk of infection. Delay
Upper right lung 11 (6) 5 (2.7) 0.125 in diagnosis and early detection of pulmonary TB is a serious
Contd... problem in Vietnam because female patients were afraid to be

44 Journal of Natural Science, Biology and Medicine ¦ Volume 9 ¦ Issue 1 ¦ January-June 2018
Icksan, et al.: MDR and DS‑TB X‑ray findings comparison

excommunicated by family and friends if they suffered from such as bronchiectasis in middle right lung. Node and
pulmonary TB.[2,4] tuberculoma on lower left lung also had a significant difference
(P < 0.005%) in MDR‑TB (4.4%) compared to DS‑TB (0).
Both MDR‑TB and DS‑TB group had most patients with age
A study by Deesuwan et al. stated that nonactive lesion found in
range from 40 to 49, 31% and 23%, respectively, with a mean
MDR‑TB was multiple bronchiectases. On contrary, this study
age of 39.87 for MDR‑TB and 41.03 for DS‑TB. In other
did not found a significant difference in multiple bronchiectasis
studies, patients’ age results were not much different.[3,4,7]
finding between MDR‑TB and DS‑TB group.
The WHO in 2013 stated that most TB patients are in their
productive age. High level of mobility and social interaction Bronchiectasis is a diffuse dilatation of multiple bronchi resulting
in productive ages supports the higher prevalence of TB due from the course of active lesion of postprimary pulmonary TB
to the increased risk of exposure.[3,4] which affects surrounding structures, for example, traction or
The large lesion was found in both MDR and DS‑TB group impaction of bronchus, bronchioles, and their branches due to
(69% vs. 27%) and showed a significant difference. Extensive recurrent reactivation. Similar to the pathogenesis of cavity
tissue damage caused by the long duration of disease is formation, nodules, or tuberculoma which do not recover will
suspected to be the reason why a lot of large lesions were found become cavity contain new pneumonia focus.[4,7,11,13]
in MDR‑TB group. A significant difference in the degree of There was no significant difference in morphology of nonactive
lesions in both groups is caused by the difference in disease pulmonary lesion between MDR‑TB and DS‑TB. For example,
progression, except in primary MDR‑TB that was caused by fibrosis in MDR‑TB and DS‑TB (23% vs. 14.8%) commonly
contaminated environment or previous interaction with the shown in upper lobe of right lung, calcification (8.2% vs. 0%)
MDR‑TB patient without any protection.[3,4,8,9] most found in mid lobe of left lung, atelectasis (1.6% vs. 3.8%)
Active lesion of lung parenchymal was found more in MDR‑TB in upper lobe of left lung, bulla (2.2% vs. 1,1%) most found
compared to DS‑TB and dominated by multiple consolidation in upper lobe of right lung, and hyper‑aeration or emphysema
and multiple cavities. Active lesion morphologies in MDR‑TB (1.1% vs. 0%) in left lower lobe of left lung. Nonactive lesion
were consolidation (57.4%), cavity (57.9%), infiltrate (36.6%), in this study has shown the possibility of reactivation.[4,7,10]
and ground glass opacity (1.1%). These active lesions were found Fibrosis and calcification are also chronic processes leading
mostly in right upper lung. Most of the lung parenchymal active to recovery.[3,4,11]
lesions in DS‑TB were also found in the upper right lung. Active There were some abnormalities outside pulmonary parenchyma
lesions for DS‑TB group were infiltrate (66.7%), consolidation that significantly different between MDR‑TB and DS‑TB
(20.8%), the cavity (6%), and ground glass opacity (2.7%). group. Those are left pulmonary effusion (19.7% vs. 2.2%),
Cavity with ≤4 cm in MDR‑TB was found most on upper right pleural effusion (7.7% vs. 1.6%), right hilum elevation
right lung (66.1%) and had a significant difference compared (19.1% vs. 2.2%), left hilum elevation (15.8% vs. 1.6%), left
to DS‑TB (14.2%) group (P < 0.005). Multiple cavities were deviation of trachea (17.5% vs. 3.3%), right deviation of trachea
found on 68.3% MDR‑TB group and had a significant difference (12% vs. 3.3%), right pleural thickening (12.6% vs. 0.5%), and
compared to 14.2% of DS‑TB group (P < 0.005). Deesuwan et al. left pleural thickening (9.8% vs. 0%). Pleural effusion found in
and Cha et al. stated that active lesions that were mostly found in this study is also accompanied by an active lesion in pulmonary
thorax X‑ray for MDR‑TB patients are multiple consolidations parenchyma, which similar result already is shown from the
and multiple cavities. Multiple reticulonodular infiltrate, ground previous study in Persahabatan Hospital. Hilum elevation,
glass opacity, and multiple or solitary cavities are the dominant tracheal deviation, and pleural thickening can occur as result
X‑ray findings for DS‑TB patients.[7,10,11] These studies support the of fibrosis in pulmonary parenchyma and pleura. These
hypothesis that the dominant characteristic lesions in MDR‑TB pleural thickening usually are the results of previous pleural
are multiple consolidations and multiple cavities (P < 0.005). All effusion.[3,4,7,10,14,15]
active lung parenchymal lesions in MDR‑TB and DS‑TB were
mostly found in the upper region of the lung. Some references The limitations of this study are the using of manual medical
stated that the dominant consolidations and cavities in MDR‑TB record and retrospective data. Therefore, many patients being
were caused by failed treatment on a postprimary TB or mutation excluded as their data were incomplete.
of MTB that caused the bacteria to be resistant to anti‑TB drugs.
These resistant bacteria might cause TB reactivation and spreads Conclusions
to the right and left lung, forming consolidation and infiltrate at In terms of lesion size, MDR‑TB group have a majority of
early stages that develop to the cavity, through the lymphatic
patients with large lesions in their chest X‑ray, meanwhile,
system, blood, or endobronchial. Unhealed cavity might cause
DS‑TB group have a dominant small‑medium lesion. In terms
new consolidations and in turn, make new cavities. Other study
of morphology, infiltrate and ground‑glass opacity were more
stated that cavities are a predisposing factor for TB treatment
dominant in DS‑TB group, whereas consolidation, cavity,
failure and reoccurrence.[4,7,11,12]
fibrosis, bronchiectasis, calcification, node, atelectasis, bullae,
Some nonlung parenchymal morphologies in the lung for emphysema, and other nonlung parenchymal findings, were
MDR‑TB and DS‑TB had a significant difference (P < 0.005), more dominant in MDR‑TB.

Journal of Natural Science, Biology and Medicine ¦ Volume 9 ¦ Issue 1 ¦ January-June 2018 45
Icksan, et al.: MDR and DS‑TB X‑ray findings comparison

Financial support and sponsorship 7. Deesuwan P, Autravisittikul O, Girapongsa L. Chest radiographic


findings of multidrug resistant pulmonary tuberculosis in comparisons
Nil. to drug‑sensitive pulmonary tuberculosis in non‑HIV patient. Region
4-5 Med J 2015;34:66‑78.
Conflicts of interest 8. Aditama TY. National Action Plan of Programmatic Management Drug
There are no conflicts of interest. Resistance Tuberculosis Control Indonesia 2011‑2014. Directorate
General for Disease and Environmental Health Control. Jakarta:
Ministry of Health Indonesia; 2011. p. 1‑54.
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