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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 11  |  Issue : 1  |  Page : 52-58

Analysis of high-resolution computed tomography chest in interferon gamma release assay negative COVID-19 patients: From a COVID hospital of Odisha, India


1 Department of Radio-Diagnosis, Kalinga Institute of Medical Sciences, Bhubaneswar, Odisha, India
2 Department of Microbiology, Kalinga Institute of Medical Sciences, Bhubaneswar, Odisha, India

Date of Submission18-Oct-2021
Date of Decision02-Dec-2021
Date of Acceptance03-Dec-2021
Date of Web Publication04-Jan-2022

Correspondence Address:
Dr. Sudhansu Sekhar Mohanty
Department of Radio-Diagnosis, Kalinga Institute of Medical Sciences, Patia, Bhubaneswar, Odisha
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijrc.ijrc_128_21

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  Abstract 


Background: Atypical category of COVID-19 could not be differentiated from tuberculosis (TB) in high-resolution computed tomography (HRCT) of the chest because of similar imaging features. This study aims to distinguish between the HRCT features of TB and atypical COVID-19. Methodology: Interferon-gamma release assay (IGRA) was performed in all the 54 COVID-positive patients, showing atypical COVID features that are suspicious of TB on the HRCT chest. Atypical imaging features such as a tree in bud nodules, patchy consolidations, cavitation with surrounding consolidation, discrete nodules, mediastinal lymphadenopathy, and pleural effusion were analyzed in 50 IGRA-negative patients. Results: We found trees in bud nodules (93%) and consolidations (56%) involving predominantly lower lobes, i.e., superior and posterobasal segments. Discrete nodules and cavitation with surrounding consolidation were seen involving predominantly upper lobes (78 and 57% cases, respectively), i.e., apicoposterior and lingular segments of the left upper lobe. The maximum number (67%) of right paratracheal enlarged nodes and bilateral pleural effusions (71%) were found in IGRA-negative COVID-19 patients. Conclusions: It is not always possible to differentiate features of atypical COVID-19 from TB based on HRCT chest alone because of similar appearances and distribution of tree in bud nodules, consolidation, cavitation, and lymphadenopathy in HRCT chest. Since both bilateral and unilateral pleural effusions may be seen in TB, it is impossible to differentiate COVID-19 from TB based on pleural effusion. Therefore, exclusion of TB will need supportive, relevant laboratory investigations (Sputum acid fast bacilli, cartridge-based nucleic acid amplification test, and IGRA) for appropriate diagnosis and management.

Keywords: Atypical COVID-19, high-resolution computed tomography chest, interferon-gamma release assay/QuantiFERON TB gold, tuberculosis


How to cite this article:
Mohanty SS, Sen KK, Mitra A, Panda S, Kuniyil J, Pattanaik D, Dubey R. Analysis of high-resolution computed tomography chest in interferon gamma release assay negative COVID-19 patients: From a COVID hospital of Odisha, India. Indian J Respir Care 2022;11:52-8

How to cite this URL:
Mohanty SS, Sen KK, Mitra A, Panda S, Kuniyil J, Pattanaik D, Dubey R. Analysis of high-resolution computed tomography chest in interferon gamma release assay negative COVID-19 patients: From a COVID hospital of Odisha, India. Indian J Respir Care [serial online] 2022 [cited 2022 Jan 29];11:52-8. Available from: http://www.ijrc.in/text.asp?2022/11/1/52/334812




  Background Top


This COVID-19 pandemic was a burden to our health care systems worldwide. Further, there has been a high prevalence of comorbid conditions such as tuberculosis (TB), especially in this part of the subcontinent where TB is considered endemic.[1] The diagnosis and treatment of TB needs to be prioritized.[2] The coexistence of TB with COVID-19 is often missed due to imaging and clinical features limitations. Typical COVID-19 can be differentiated from TB with high-resolution computed tomography (HRCT) Chest. However, atypical COVID-19 features like a tree in bud nodules, consolidation, cavitation, pleural effusion, and mediastinal lymphadenopathy could also represent TB.[3],[4]

This study aims to analyze the imaging features of atypical COVID-19, indicative of suspected association of pulmonary TB in COVID-19 patients. We also assessed the imaging features in Interferon-gamma release assay (IGRA)-negative COVID patients and tried to differentiate between COVID-19 and TB based on HRCT chest.


  Methodology Top


This is a cross-sectional hospital-based study conducted over a period of 6 months from July 1, to December 31, 2020 in a COVID Hospital, Odisha, India, after approval from the institutional ethical committee. During this period, 50 consecutive cases had an atypical category of COVID features mimicking TB and were found to be IGRA negative, and those cases were selected as our study sample. Our study included all three categories (mild, moderate, and severe) of patients based on clinical severity. Those COVID patients who were not showing any findings suspicious of TB in HRCT chest, those who were not undergone IGRA test, and those who were found to be IGRA positive were excluded from this study. Also, patients who showed positive blood investigations for other infective and inflammatory etiologies and showed atypical features on the HRCT chest were excluded from our study.

HRCT chest scans of all the 54 patients were performed with 64 Slice computed tomography (CT) scanner (Siemens-Somatom: Go up) with SAFIRE software. Scans were acquired in a single breath-hold. Scanning parameters were 120 kV, 150 mA, and 5 mm slice thickness with reconstruction to 0.65 mm. HRCT thorax images were analyzed using standard lung (window width 1500 HU; window level– 600 HU) and mediastinal (window width 350 HU; window level 40 HU) window settings. HRCT Chest findings that were suspicious for TB, like tree in bud nodules, multiple discrete randomly arranged nodules, consolidation, cavitation, pleural effusion, and mediastinal lymphadenopathy were recorded along with their pattern segmental distribution.

Hence to rule out TB in these COVID-19 patients, a QuantiFERON TB gold (QFT) enzyme-linked immunosorbent assay (ELISA)/IGRA test was performed.

Principle of interferon-gamma release assay

These are blood tests of a cell-mediated immune response, and they measure the T-cell release of (INF)-Gamma following stimulation by antigens specific to the Mycobacterium tuberculosis complex (with the exception of BCG substrains), i.e., early secreted antigenic target 6 and culture filtrate protein 10.[5] These antigens are encoded by genes located within the region of difference 1 locus of the M. tuberculosis genome and are more specific than purified protein derivative for M. tuberculosis.[6] Two types of IGRAs are available: QuantiFERON-TB assay (whole blood ELISA), which measures the concentration of INF-gamma secretion, and the T-SPOT. TB assay (ELISpot) directly counts the number of INF-gamma secreting T-cells. Both are approved by the US Food and Drug Administration.[6] In our study, QuantiFERON-TB assay (whole blood ELISA) is used to rule out TB.

Technique of QuantiFERON-TB assay (whole blood ELISA).

Before collecting the blood sample in Heparin tubes for the IGRA test, written consent was taken from all the patients. Approximately 2.5–3 ml of blood is collected in heparin tubes, and then this heparinized blood is transferred into three tubes containing either TB antigens, mitogen, or nothing (negative control). Each tube should contain ~0.8–1.2 ml of blood. Then these tubes are shaken ten times to mix well, followed by incubation at ~37+/-1°C. After incubation, tubes may be stored at 4–27°C before centrifugation. The tubes can be directly centrifuged without any storage. After centrifugation, the supernatant is taken for the ELISA test. An individual is considered positive for M. tuberculosis infection if the INF-gamma response to TB antigens is above the test cut-off (after subtracting the background INF-gamma response in the negative control). The result is expressed in IU/ml.[7]

According to a study done by Takasaki et al.,[8] in 99 patients of confirmed active TB, sensitivity, and specificity of QuantiFERON-TB assay (whole blood ELISA) were found to be 98.9% (95% confidence interval [CI],0.934-0.998) and 98.1%; (95% [CI], 0.934-0.998) respectively. Therefore, IGRA has more specificity and sensitivity than tuberculin skin test (TST)/Mantoux test in detecting TB infection in BCG vaccinated people. IGRA gives fewer false-positive results than TST, as it detects only M. tuberculosis, whereas TST also detects nontuberculous mycobacterium along with M. tuberculosis.[9],[10],[11]

QFT/interferon-gamma release assay test was preferred over cartridge-based nucleic acid amplification test in our study for the following reasons

  1. COVID-positive patients were admitted to the COVID ward. To protect the inexperienced, apprehensive, and reluctant health workers from the hazards of COVID infection during the collection of a sputum sample, IGRA was a better choice over cartridge-based nucleic acid amplification test (CBNAAT).
  2. Sputum needs to be collected properly to avoid contamination with saliva. A standard procedure called 'Sputum induction' is followed. Sputum induction is done after inhalation of nebulized sterile saline solution (isotonic or hypertonic) followed by coughing and expectoration of airway secretions.[12] But due to the enormously rising patient load in our COVID hospital and the paucity of skilled health workers in the COVID ward, this technique couldn't be followed for sputum sample collection leading to sub-optimal sample collection most instances. Therefore, IGRA was the other alternative, considering the perpetually increased risk of COVID cross infection to health workers and to avoid improper and suboptimal sample collection in the COVID ward.


Statistical analysis

Data were entered and analyzed using MS office excel 2019. Descriptive statistics were applied, and categorical variables were expressed in percentages.


  Results Top


In our study, out of 54 patients showing HRCT chest findings suspicious of TB, 50 (93%) were IGRA negative, and 4 (7%) were IGRA positive. Out of 50 IGRA-negative patients, 16 (32%) were females, and 34 (68%) were males. In our study group number of patients belonging to different age groups, i.e., from 21 to 30, 31–40, 41–50, 51–60, 61–70, and 71–80 years were 4, 7, 7, 14, 8, and 10 respectively [Figure 1]. Distribution of Atypical features in IGRA-negative COVID patients as shown the [Table 1].
Figure 1: Age-wise distribution of COVID patients with atypical HRCT chest features

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Table 1: Distribution of atypical COVID features in interferon-gamma release assay-negative COVID patients

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High-resolution computed tomography chest: Atypical features in interferon-gamma release assay-negative COVID patients

Distribution

Tree in bud nodules

Upper lobes were involved in 12 (80%) out of 15 cases, including the right upper lobe in 5 cases, the left upper lobe in 5 cases, and the bilateral upper lobes in 1 case. Lower lobes were involved in 14 (93%) cases, out of which right lower lobes in 7 cases, left lower lobes in 5 cases, and bilateral lower lobes in 1 case. In 6 (40%) cases, the right middle lobe was involved. In 1 case, both upper and lower lobes were involved [Table 2]a and [Table 2]b. Most of the patients were showing a tree in bud nodules in multiple lobes. In 4 cases, more than one lobe was involved [Table 3].


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Table 3: Multi-lobar involvement of atypical lesions in both lungs

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Consolidation

Out of 16 cases with consolidations, upper lobes were involved in 3 (19%) cases, all of which are left upper lobes. Lower lobes were involved in 9 (56%) cases. Out of 9 cases, the right lower lobe was involved in 4 cases, the left lower lobe in 3 cases, and bilateral lower lobes in 2 cases. The middle lobe was involved in 3 (19%) cases [Table 2]a and [Table 2]b. All lobes were involved in one case [Table 3].

Cavitation with surrounding consolidation

Upper lobes were involved in 7 (78%) out of 9 cases. Out of these 7 cases, the left upper lobe was involved in 5 cases, and the right upper lobe was involved in 2 cases. The right middle lobe was involved in 2 (22%) cases. Lower lobes were involved in 3 (33%) cases, out of which in 1 case both right (medial basal segment) and left (posterior basal segment) lower lobes were involved, and in the remaining 2 cases, right lower lobes (posterior basal and superior segments) were involved [Table 2]a and [Table 2]b. 3 cases showed cavitation with surrounding consolidation in more than one lobe [Table 3].

Discrete nodules

Multiple randomly arranged discrete nodules were seen in upper lobes in 4 (57%) out of 7 cases. Lower lobes were involved in 3 (43%) cases. The middle lobe was involved in 3 (43%) cases. All lobes were involved in 1 case [Table 2]a and [Table 2]b. Maximum size of nodule measured ~1.6 cm in size. More than one lobe is involved in 4 cases [Table 3].

Mediastinal lymphadenopathy

Out of 9 cases, right paratracheal nodes were seen in 6 (67%) cases, whereas left paratracheal, aortopulmonary window, precarinal, subcarinal, pretracheal, and prevascular nodes were seen in the rest of the 3 cases. The largest node diameter measured ~2.4 cm in short-axis diameter in the right paratracheal location.

Pleural effusion

Out of 14 cases, bilateral pleural effusion was seen in 10 (71%) cases and unilateral in 4 (29%) cases (2 on each side).

Mixed pattern

Tree in bud nodules with patchy consolidations was noted in 10 (20%) cases and consolidation with cavitation in 8 (16%) cases. All the three patterns like a tree in bud nodules, cavitation, and consolidation were seen in 5 (10%) cases [Table 1].


  Discussion Top


The atypical category of COVID-19 shows a tree in bud nodules, consolidation, cavitation, discrete nodules, pleural effusion, and mediastinal lymphadenopathy in the HRCT chest, which are also seen in TB. Therefore, differentiation between atypical COVID-19 and TB is not always possible based on imaging. This often delays early specific management of TB along with COVID-19 protocol. Our study has tried to differentiate the features of atypical COVID-19 from that of TB with certainty, correlating with the IGRA results.

Our study population consists of more males than females. The maximum number of patients belong to 51–60 years' age group followed by 71-80 years, suggesting that atypical COVID features are seen predominantly in elderly patients. The mean age was found to be 53 years. This is in accordance with a study done by Jin et al., which concluded that atypical features were more common in elderly patients.[13] Maximum numbers of atypical features were found to be consolidation (32%), followed by a tree in bud pattern (30%) and pleural effusion (28%) in our study population.

Tree in bud nodule pattern is due to dilatation of centrilobular bronchioles and filling up these bronchioles with mucus, pus, or fluid and usually seen in peripheral aspect of lungs.[14] It suggested the early bronchogenic spread of infection and was initially described as only associated with TB.[15],[16] However, it is also described in other bacterial, fungal, viral, or parasitic infections, congenital disorders (Kartagener's syndrome and cystic fibrosis), idiopathic diseases (obliterative bronchiolitis, and panbronchiolitis), aspiration, toxic fume inhalation, immunologic disorders (like ABPA), and connective tissue disorders (like RA), peripheral pulmonary vascular diseases and neoplastic pulmonary emboli.[17],[18] Typically, they appear as 2-4 mm sharp well defined linear branching nodules around terminal bronchioles in CT.[15] [Figure 2] In our study, we found a tree in bud nodules that were tiny (measuring ~2–4 mm in size), well defined, sharply marginated, and involving superior segments of lower lobes in a maximum number of cases (i.e., 6 out of 14 (43%) cases), followed by upper and middle lobes. Among upper lobe involvement, entire right upper lobe involvement was found in a maximum number of cases (i.e., 4 out of 14 (28%) cases) as shown in [Table 2]a and [Table 2]b. Similarly, consolidations [Figure 3] were found in posterior basal segments of lower lobes in a maximum number of cases (i.e., 4 out of 16 (25%) cases) as shown in [Table 2]a and [Table 2]b. According to a study done by Song et al., ground-glass opacities (GGO) and consolidations in more than 90% cases of COVID-19 were seen in lower lobes.[19] In another study by Shi H et al., lower lobes were more commonly involved in COVID-19 by GGOs and consolidations.[20] Therefore, our study is consistent with these studies suggesting findings in favor of COVID-19. However, [Table 3] shows multilobar involvement of all the atypical features. According to Yeh et al., multiple segmental involvements of consolidations are more likely to have smear-positive sputum acid fast bacilli (AFB) test.[21]
Figure 2: (a) Axial mediastinal window showing left mild and right minimal pleural effusions (red arrows) with underlying collapse consolidation in left lower lobe and mediastinal lymphadenopathy (orange arrow). (b) Axial lung window showing a tree in bud nodules (yellow arrows) in bilateral upper lobes (L > R)

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Figure 3: (a) Axial mediastinal and (b) Axial lung window images showing consolidation with multiple air bronchograms in posterobasal and medial basal segments of the right lower lobe (red arrows)

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According to Bhalla et al., tree in bud nodules and consolidations involving apical and posterior segments of right upper lobe, an apicoposterior segment of left upper lobe and right middle lobe, lingula, and superior segment of any lower lobe are suggestive of active TB.[22] Although lower lobe predominance of TIB nodules and consolidation was noted in our study, due to the involvement of apicoposterior and lingular segments of left upper lobe, right middle lobe, and superior segment of lower lobe, an association of TB couldn't be ruled out. We also found maximum numbers of patients (14 (66%) out of 21) of 61-80 years age group showing consolidations with lower lobar predominance in this study. Hence, this was inconsistent with a study done by Yeh et al., in which they concluded that basal segmental consolidations in elderly patients might be associated with TB.[23] In our study, as the IGRA test had already ruled out TB, all these findings were either due to COVID-19 itself or due to other differential diagnoses as described earlier, which need to be ruled out.

Multiple randomly arranged discrete nodules were more prevalent in the upper lobes in our study. [Table 2]a and [Table 2]b show involvement of apicoposterior and lingular segments of left upper lobe, anterior and posterior segment of right upper lobe, a lateral segment of right middle lobe and entire right middle lobe, posterobasal segment of left lower lobe, and superior segments of bilateral lower lobes with a maximum number of cases involving an apicoposterior segment of left upper lobe in 3 out of 7 (43%) cases and upper lobes in 4 out of 7 (57%) cases. According to Yeh et al. and El-Solh et al., nodules, cavitations, and consolidations in the upper lobes were suggestive of active TB in several prediction models.[23],[24] In our study, after ruling out TB by IGRA test, these nodules are either due to COVID-19 itself or due to other differential diagnoses like infectious conditions (fungal, viral, and septic emboli), inflammatory conditions (like Sarcoidosis, RA) and neoplastic etiology (metastasis, lymphoma).[25] We found multiple discrete nodules randomly arranged in bilateral lungs in one case, which was found to be metastatic lesions from carcinoma thyroid.

Cavities may develop in the late recovery phase of COVID patients.[26],[27],[28],[29] cavitation is due to diffuse alveolar damage, alveolar hemorrhage followed by necrosis of lung parenchyma.[30],[31] In our study, cavities with surrounding consolidations predominantly involved upper lobes followed by middle and lower lobes.[Figure 4] We found cavitations predominantly involving apicoposterior and lingula of left upper lobe (5 out of 9 (55%) cases) and apical and posterior segments of right upper lobe (2 out of 9 (22%) cases) along with medial and lateral segments of right middle lobe and superior segment of right lower lobe simulating active TB.[23],[24],[32],[33] After screening out TB by IGRA test, cavitations with surrounding consolidation could be either due to COVID-19 or due to other bacterial infections (like Streptococcus pneumoniae, Staphylococcus aureus, Klebsiella pneumoniae, and H. influenzae), fungal (like aspergillosis), nontuberculous mycobacterium and parasites.[34]
Figure 4: (a) Axial mediastinal and (b) Axial lung window images showing cavitation with surrounding consolidation in apicoposterior segment of left upper lobe (blue arrows) and right mild pleural effusion (red arrow)

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Among all cases of mediastinal lymphadenopathy [Figure 2], we found right paratracheal enlarged nodes in a maximum number of cases. According to Garg and Kalra, right paratracheal nodes were most commonly enlarged in TB in India.[35]

Our study found more IGRA-negative patients with bilateral pleural effusions (71%) than unilateral pleural effusion (29%) [Figure 2] and [Figure 4]. According to Bomanji, et al., unilateral pleural effusion may present alone in adult-onset primary TB.[4] Therefore, bilateral pleural effusion in COVID patients points more toward COVID infection in the absence of other comorbid conditions like renal, hepatic, and cardiac diseases.

Limitations

IGRA cannot differentiate between active and latent TB. Immunocompromised patients may show false-negative IGRA test. A negative IGRA test does not exclude the possibility of M. tuberculosis infection. If the sample is taken before developing an immune response, false-negative results may be obtained. We have not ruled out other differential diagnoses of TB in our study.


  Conclusion Top


Atypical COVID features are more prevalent in elderly males, and the most common age group is 51–60 years, with a mean age of 53 years.

Although tree in bud nodules and consolidations are predominantly seen in lower lobes, i.e., superior and posterior basal segments respectively in IGRA-negative COVID-19 patients, because of similar nature of tree in bud nodules and consolidations, similar segmental involvement as that of TB and also because of multi-segmental distribution, the possibility of TB cannot be ruled out based on imaging.

Due to similar segmental involvement of other atypical features like discrete nodules and cavitation with surrounding consolidation in HRCT chest cannot differentiate atypical COVID-19 from TB.

Although bilateral pleural effusions are more prevalent in IGRA-negative COVID-19 patients than unilateral, TB cannot be ruled out based on laterality as bilateral effusions may be seen in TB.

As right para-tracheal lymphadenopathy is seen predominantly in IGRA-negative COVID patients and TB, it is impossible to differentiate between them in imaging-based on lymphadenopathy.

Hence, we conclude that the atypical category of COVID-19 can mimic TB on imaging, especially in the developing countries where the disease is considered endemic, and it is not possible to differentiate features of atypical COVID-19 from TB based on HRCT Chest alone. Hence the exclusion of TB will need supportive, relevant laboratory investigations (Sputum AFB, CB NAAT, and IGRA) for appropriate management.

Acknowledgments

Authors are very much thankful to Director General & Principal, KIMS, Dr. (Col) Pradeep Kumar Pattanaik, for his continued support for the study. We are also thankful to Mrs. Kavita Baral, the Assistant Nursing Superintend, Mr. Debadutta Sahoo, Laboratory Manager and all the staffs working in COVID hospital, who helped in collection and transfer of the blood samples to the laboratory.

Financial support and sponsorship

This study was supported financially by Kalinga Institute of Medical Sciences (KIMS), Bhubaneswar, Odisha, India.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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Abstract
Background
Methodology
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