A diagnosis of coronavirus disease 2019 (COVID-19) is made on the basis of epidemiological and clinical history, as well as the results of severe acute respiratory syndrome coronavirus 2 real-time reverse transcriptase polymerase chain reaction (RT-PCR) testing. Chest computed tomography (CT) has been proposed as a useful alternative investigation method for COVID-19 diagnosis or triage, particularly in healthcare settings with restricted access to RT-PCR testing and in the context of lower RT-PCR sensitivity during early stages of the disease; it may also be useful for imaging-mediated evaluation of disease severity and progression.1 2 The most common CT findings in early-stage COVID-19 pneumonia (illness days 0-5) are pure ground-glass opacities (GGOs); the second most common finding is consolidation.3 4 In the later stages (illness days 6-17), findings usually evolve to a combination of GGOs, consolidation, and reticular opacities with architectural distortion.4 These imaging features are not specific to COVID-19 pneumonia; they can overlap with other types of viral or bacterial pneumonia, particularly influenza pneumonia, as well as other non-infectious inflammatory lung diseases.5 6 Influenza, one of the most common causes of viral pneumonia,7 and bacterial pneumonia, historically the most common type of community-acquired pneumonia worldwide,8 maintained high incidences during the early COVID-19 pandemic when this study was conducted; thus, they had the potential to substantially contribute to hospitalisations in this period. However, COVID-19 pneumonia and other types of viral or bacterial pneumonia distinctly differ in terms of their disease course, temporal progression, and available therapeutics9 10 11; thus, there is a need for early and accurate differentiation among these entities.

Studies in 2020 revealed several CT imaging features that can aid in differential diagnosis. Compared with influenza pneumonia, patients with COVID-19 pneumonia are more likely to exhibit a peripheral distribution,12 13 14 patchy combination of GGOs and consolidation,15 fine reticular opacities,16 and vascular thickening or enlargement16 17; patients with influenza pneumonia are more likely to exhibit nodules,18 tree-in-bud sign,18 bronchial wall thickening,15 lymphadenopathy,16 and pleural effusions.12 In the past, diffuse airspace consolidation, centrilobular nodules, bronchial wall thickening, and mucous impaction19 have been identified as typical signs of bacterial pneumonia. Nevertheless, CT assessment of COVID-19 generally remains challenging, with reported accuracies for radiologists ranging from 60 to 83%16 in terms of differentiating patients with COVID-19 pneumonia from patients with influenza pneumonia; considering these rates, further studies of relevant imaging findings are needed.

A report by Wu et al20 highlighted the arched bridge sign, which may be a distinct CT feature of COVID-19 pneumonia. In their analysis of 11 patients with COVID-19 pneumonia, the sign was present in 72.7%.20 The arched bridge sign refers to a specific pattern of GGOs or consolidation, commonly in a subpleural location, which forms an arched contour with a smooth concave margin towards the pleural side. The arched margin outlines the spared parenchyma between the GGOs or consolidation and the pleural surface. Another reported sign, regarded as the vacuole sign,21 22 23 24 is presumably based on the morphological pattern of parenchymal sparing in areas of affected lung. The vacuole sign refers to a focal oval or round lucent area (typically <5 mm) that is observed within GGOs or sites of consolidation. In clinical practice, we often observed these two novel signs on CT scans of patients with COVID-19 pneumonia. We hypothesised that these two signs are common in patients with COVID-19 pneumonia and thus could be used to differentiate such pneumonia from other types of infection-related pneumonia. However, considering the limited prior evidence (solely from small retrospective studies20 21 22 23 24) regarding the prevalence of the vacuole sign in COVID-19 pneumonia, and because the arched bridge sign has—to our knowledge—only been reported in a single previous publication,20 additional assessments of these signs are needed. The utilities of the arched bridge and vacuole signs in COVID-19 pneumonia have not been directly assessed in prior reports, nor have they been compared between COVID-19 pneumonia and other types of infection-related pneumonia. In this study, we evaluated the arched bridge and vacuole signs in patients with COVID-19 pneumonia, then examined whether these signs could be used to differentiate such pneumonia from influenza pneumonia or bacterial pneumonia.

This retrospective study included consecutive patients who were admitted to two hospitals in Hong Kong (Prince of Wales Hospital and Princess Margaret Hospital) with RT-PCR–confirmed COVID-19, along with positive CT findings, from 24 January 2020 to 16 April 2020. These patients represent most patients with COVID-19 in Hong Kong during the study period, when all patients with confirmed COVID-19 were hospitalised regardless of clinical status; moreover, Princess Margaret Hospital also served as a centralised treatment centre for patients with COVID-19. The study recruitment period reflects the early days of the COVID-19 pandemic in Hong Kong, during which CT examinations were commonly performed during the diagnosis and treatment of patients with COVID-19. All patients with COVID-19 underwent complete PCR-based assessment of multiple respiratory pathogens on admission; patients with COVID-19 were excluded from the present study if they exhibited evidence of other concomitant viral or bacterial respiratory infections.

The influenza pneumonia and bacterial pneumonia comparison groups comprised consecutive patients who were admitted to Prince of Wales Hospital in Hong Kong, with pure influenza pneumonia or pure bacterial pneumonia and positive CT findings from 20 February 2018 to 13 January 2020. The diagnosis of pure influenza pneumonia was determined by RT-PCR–mediated detection of influenza A or B viral RNA, in the absence of evidence (eg, respiratory or blood cultures, PCR tests, or serological tests) suggesting concomitant infection with other viral or bacterial pathogens. The diagnosis of pure bacterial pneumonia was determined by positive bacterial culture on sputum or bronchoalveolar lavage, in the absence of evidence suggesting concomitant infection with other viral or bacterial pathogens. Patients with pre-existing lung parenchymal disease (eg, interstitial lung disease) or known lung malignancy were excluded from the study.

Computed tomography scans were performed using 64-section multidetector scanners (LightSpeed VCT or LightSpeed Pro 32, GE Medical Systems, Milwaukee [WI], United States). The following scan parameters were used: voltage, 120 kV; tube current, 50-502 mA; and slice thickness, 0.625 mm or 1.25 mm. Scans were performed with the patient in the supine position during end-inspiration.

All CT images were reviewed in random order by two trained radiologists (TY So and YX Wang) with 7 and 5 years of experience in diagnostic chest imaging, respectively, using a dedicated picture archiving and communication system workstation. Each radiologist was blinded to demographic and clinical information for all patients. The images were independently reviewed by each radiologist, and the consensus findings for any discrepancies from discussion are reported.

Each CT image was initially subjected to broad assessment of abnormalities. Subsequently, the arched bridge and vacuole signs were specifically assessed; the presence or absence of each sign was recorded. The arched bridge sign was defined as the presence of GGOs or consolidation with an arched concave margin outlining a region of spared lung; the vacuole sign was defined as the presence of a vacuole-like region of normal lung (<5 mm) within GGOs or sites of consolidation.21

For patients with COVID-19 pneumonia and patients with influenza pneumonia, CT findings of GGOs (hazy areas of parenchymal opacities that did not conceal underlying vessels), consolidation (parenchymal opacities that concealed underlying vessels), reticular opacities (coarse linear or curvilinear opacities, interlobular septal thickening, or subpleural reticulation), and crazy paving pattern (GGOs with interlobular and intralobular septal thickening) were recorded. Other signs such as air bronchograms (air-filled bronchi on a background of opaque lung), nodules (small rounded focal opacities <3 cm), cavitation (gas-filled spaces within sites of pulmonary consolidation), bronchiectasis, pleural retraction or thickening, pleural effusion, pericardial effusion, pneumothorax, and mediastinal lymphadenopathy (lymph nodes >1 cm in short-axis diameter) were also recorded. The distributions of pulmonary abnormalities were classified as unilateral or bilateral, and peripheral (involving mainly the peripheral one-third of the lung), central (involving mainly the central two-thirds of the lung), or diffuse (involving both peripheral and central regions). Lobar involvement was also recorded (right upper lobe, right middle lobe, right lower lobe, left upper lobe, and/or left lower lobe). For patients with bacterial pneumonia, only the arched bridge and vacuole signs were recorded. Other CT changes and their distributions were not individually recorded. This component of the analysis was determined based on reports that it is easier to differentiate COVID-19 pneumonia from bacterial pneumonia, whereas it is more difficult to differentiate COVID-19 pneumonia from other types of viral pneumonia.6 25 26 This manuscript was written in accordance with the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines for reporting observational studies.

Imaging findings were compared using the Chi squared test or Fisher’s exact test, as appropriate, followed by Bonferroni correction. Comparisons of disease stage, severity, and clinical course among patients with COVID-19 who had the arched bridge and/or vacuole signs were performed using the non-parametric Mann-Whitney U test. P values <0.05 were considered indicative of statistical significance. For the arched bridge and vacuole signs, the sensitivity, specificity, positive predictive value, and negative predictive value were calculated, along with the respective 95% confidence intervals. All analyses were conducted using SPSS software (Windows version 25.0; IBM Corp, Armonk [NY], United States).

Among 76 patients with bacterial pneumonia who were admitted for treatment during the study period, five patients with pre-existing lung parenchymal disease were excluded from the analysis: organising pneumonia (n=2), non-specific interstitial pneumonia (n=1), and idiopathic interstitial pneumonia of uncertain subtype (n=2). No patients with COVID-19 required exclusion because of concomitant viral or bacterial infections. The final study population comprised 187 patients: 66 patients with COVID-19 pneumonia, 50 patients with influenza pneumonia, and 71 patients with bacterial pneumonia. The following organisms were detected in patients with bacterial pneumonia: Streptococcus pneumoniae, Staphylococcus aureus, Haemophilus influenzae, Enterococcus spp., Klebsiella pneumoniae, Pseudomonas aeruginosa, Escherichia coli, Stenotrophomonas spp., Serratia spp., Acinetobacter spp., and Moraxella catarrhalis. Demographic and clinical characteristics of the study population are shown in Table 1. Compared with patients in the influenza pneumonia and bacterial pneumonia groups, patients with COVID-19 pneumonia tended to be younger and healthier.

The arched bridge and vacuole signs were present in 42 (63.6%) and 14 (21.2%) of 66 patients with COVID-19 pneumonia, respectively (Table 2). The arched bridge sign was commonly in a subpleural location, and there was a smooth arched margin outlining the underside of the GGO or consolidation in all cases (Fig a and b). The vacuole sign was present with GGOs or sites of consolidation in various locations (Fig c and d). The arched bridge sign was much more common in patients with COVID-19 pneumonia than in patients with influenza pneumonia (63.6% vs 8.0%) or bacterial pneumonia (63.6% vs 5.6%, P<0.001). Similarly, the vacuole sign was much more common in patients with COVID-19 pneumonia than in patients with influenza pneumonia (21.2% vs 2.0%, P=0.005) or bacterial pneumonia (21.2% vs 1.4%, P<0.001).

The arched bridge and vacuole signs occurred together in 11 (16.7%) of 66 patients with COVID-19 pneumonia, but they did not occur together in any patients with influenza pneumonia or bacterial pneumonia. Additionally, a review of the five excluded patients with bacterial pneumonia and concurrent pre-existing lung parenchymal disease revealed that none of those patients exhibited the arched bridge sign or the vacuole sign.

In this study, the arched bridge and vacuole signs exhibited high specificities (93.4% and 98.4%, respectively) in terms of identifying COVID-19 pneumonia (Table 3), with moderate or low sensitivities (63.6% and 21.2%, respectively). They also exhibited high positive predictive values (84.0% and 87.5%, respectively) and high or moderate negative predictive values (82.5% and 69.6%, respectively).

The relationships of the arched bridge and vacuole signs with disease course are shown in Table 4. Computed tomography was mainly performed during admission, at a mean of 5.3 days after admission, suggesting these two signs generally appeared at an early stage. Comparisons of patients with COVID-19 pneumonia who had and did not have these two signs revealed that the arched bridge sign was associated with more extensive lung involvement (diseased lobes: 4.0 [present] vs 2.4 [absent], P<0.001). This trend was not evident for the vacuole sign (diseased lobes: 3.8 [present] vs 3.3 [absent]). There was no significant difference in the duration of total hospitalisation between patients with COVID-19 who had and did not have these two signs, suggesting they were not associated with a better or worse prognosis if appropriate treatment was administered.

Table 5 shows the comparison of other CT findings between COVID-19 pneumonia and influenza pneumonia. No significant differences were observed in the incidences of GGOs, consolidation, reticular opacities, or crazy paving between patients with COVID-19 and patients with influenza pneumonia (all P>0.05). Air bronchograms (P=0.003), nodules (P=0.009), cavitation (P=0.004), bronchiectasis (P<0.001), pleural effusion (P<0.001), pericardial effusion (P=0.032), and mediastinal lymphadenopathy (P<0.001) were significantly more common in patients with influenza pneumonia.

Abnormalities were more commonly bilateral in patients with COVID-19 pneumonia (77.3%) and patients with influenza pneumonia (96%). The distribution was more likely to be peripheral in patients with COVID-19 pneumonia (51.5% vs 2.0%, P<0.001), and was more likely to be diffuse in patients with influenza pneumonia (98% vs 48.5%, P<0.001). The right upper lobe (P<0.001), right middle lobe (P<0.001), and left upper lobe (P<0.001) were less commonly involved in patients with COVID-19 pneumonia than in patients with influenza pneumonia.

This study evaluated the incidences and diagnostic values of the arched bridge and vacuole signs among patients with COVID-19 pneumonia in a Hong Kong Chinese population. Since the initial description of Wu et al20 in a series of 11 patients with COVID-19, our study is the first to validate the arched bridge sign in patients with COVID-19. To our knowledge, this is also the first study to evaluate the vacuole sign in non–COVID-19–related pneumonia. The arched bridge sign was significantly more common in COVID-19 pneumonia than in influenza pneumonia or bacterial pneumonia. Additionally, the incidences of the vacuole sign and both signs observed in combination were higher (or tended to be higher) in patients with COVID-19 pneumonia than in patients with influenza pneumonia or bacterial pneumonia. Our results imply that these two signs generally appeared at an early stage; the arched bridge sign is more likely to be observed in patients with more severe lung pathology. These results suggest that the arched bridge and vacuole signs can be used in CT-based identification of COVID-19 pneumonia, as well as efforts to differentiate COVID-19 pneumonia from other types of infection-related pneumonia. Currently, chest CT is not recommended for the screening or diagnosis of COVID-19 pneumonia when RT-PCR tests are available. In selected cases, CT can be used to monitor clinical progress and identify complications of the disease. In some scenarios, CT can be a useful alternative investigation method for COVID-19 diagnosis or triage, such as healthcare settings with restricted access to RT-PCR tests.27 28 When these two signs are observed on CTs performed for COVID-19 pneumonia or other indications during the COVID-19 pandemic, physicians should carefully consider a diagnosis of COVID-19 pneumonia. However, our findings indicated there was no significant difference in the duration of total hospitalisation between patients with COVID-19 pneumonia who had and did not have these two signs, suggesting that they are not indicative of a better or worse prognosis if appropriate treatments are administered.

The underlying pathophysiological mechanisms behind these signs remain unclear. However, the morphological appearances of the arched bridge and vacuole signs may indicate different pathophysiological mechanisms of lung sparing that occur during infection-related pneumonia. Histopathological examinations of lung biopsy tissues from patients with COVID-19 pneumonia have provided evidence of variations in diffuse alveolar damage.29 30 The curved concave margin in the arched bridge sign may be the result of secondary pulmonary lobule sparing, with the interlobular septum of the secondary pulmonary nodule forming some resistance to the spread of infection among lobules.20 In contrast, the vacuole sign (ie, a very small focal lucent area) may reflect a spared alveolar cluster or dilated alveolar sac within an area of otherwise involved lung.21 23 Zhang et al23 reported that the vacuole sign was often present in patients with advanced COVID-19 pneumonia, where alveolar sac dilation could result from damage to the alveolar wall.

The incidence of the arched bridge sign in patients with COVID-19 (63.6%) was similar to the incidence reported by Wu et al20 (72.7%). The incidence of the vacuole sign (21.2%) in patients with COVID-19 pneumonia is also within the range reported in prior studies describing this sign (17-66%).21 22 23 24 Notably, three additional case series have revealed spared airspaces in patients with COVID-19 pneumonia, comprising ‘round cystic changes’31, ‘cystic air spaces’32 and ‘cavity signs’,33 with prevalences of 10 to 30%; these phenomena may include the vacuole sign. However, these case series did not include formal definitions of the findings. The differences in definitions of the vacuole sign (and phenomena that include the sign) may also explain the disparate prevalences (17%-66%, as noted above) reported in the literature.

The arched bridge and vacuole signs differentiated COVID-19 pneumonia from influenza pneumonia and bacterial pneumonia with high specificities and high positive predictive values, suggesting that these signs can help to provide a specific imaging diagnosis of COVID-19 pneumonia. When encountering inconclusive CT features of COVID-19 pneumonia, these signs can be identified with minimal additional effort; their presence may be sufficient to increase suspicion or add to the evidence confirming a diagnosis of COVID-19 pneumonia. The respective sensitivities of the arched bridge and vacuole signs were moderate (63.6%) and low (21.2%); the arched bridge sign may be more useful in this context. Our findings suggest that the combined presence of the arched bridge and vacuole signs strongly supports a diagnosis of COVID-19 pneumonia.

Consistent with previous studies, the presence of nodules, cavitations, bronchiectasis, pleural effusion, pericardial effusion, and/or mediastinal lymphadenopathy was uncommon in patients with COVID-19 pneumonia; these features were more common in patients with influenza pneumonia.12 16 17 18 34 35 Our results indicated that COVID-19-related abnormalities on CT were generally bilateral and peripheral, compatible with the findings in prior studies.12 13 14

This study had several limitations. First, it used a retrospective design, and patients were imaged in a cross-sectional manner at various time intervals after symptom onset. Computed tomography was not regularly performed, which hindered the monitoring or analysis of imaging signs over time. Second, CT was not routinely performed for patients with influenza pneumonia or bacterial pneumonia; it was performed based on clinical judgement, generally because of patient deterioration or poor response to treatment. We did not assess differences in the clinical features of patients with influenza pneumonia and patients with bacterial pneumonia between patients who did and did not undergo CT. Third, we attempted to implement diversity in our analysis of COVID-19 pneumonia by comparisons with influenza pneumonia and bacterial pneumonia, whereas prior studies have generally been limited to comparisons of COVID-19 pneumonia with influenza pneumonia. However, we did not examine other types of viral pneumonia; we also did not conduct subgroup analysis according to influenza subtype. Additionally, we did not systematically compare the prognoses of patients with non–COVID-19 pneumonia who had and did not have the arched bridge or vacuole signs. This comparison was hindered by the sample size, because these two signs were very uncommon in patients with non–COVID-19 pneumonia. However, additional analysis did not reveal a clear pattern whereby these two signs would be predictive for clinical prognosis in patients with non–COVID-19 pneumonia. Finally, the sample size in this study was moderate. Although the prevalences of the arched bridge and vacuole signs in our patients with COVID-19 pneumonia were consistent with findings in the literature, their diagnostic specificities should be validated in other types of pneumonia. Despite these limitations, the high diagnostic specificities of these CT signs provide insights that will be useful in future studies. Additional work is needed regarding the relationships of these CT signs with clinical status, and our findings require validation in larger and more diverse patient populations.

In conclusion, two morphological patterns of lung sparing, namely the arched bridge and vacuole signs, are much more common in patients with COVID-19 pneumonia; they have the potential to differentiate COVID-19 pneumonia from influenza pneumonia and bacterial pneumonia. In this study, these signs had high specificities and positive predictive values for COVID-19 pneumonia. The identification of these signs in clinical practice may be useful for increasing suspicion or providing confirmatory evidence to support a diagnosis of COVID-19 pneumonia.

Concept and design: TY So, SCH Yu, JYX Wang.
Acquisition of data: All authors.
Analysis and interpretation of data: All authors.
Drafting of the manuscript: TY So, S Yu, JYX Wang.
Critical revision of the manuscript for important intellectual content: All authors.

All authors had full access to the data, contributed to the study, approved the final version for publication, and take responsibility for its accuracy and integrity.

The authors have no conflicts of interest to disclose.

The authors thank Ms Apurva Sawhney, Department of Imaging and Interventional Radiology, The Chinese University of Hong Kong, for assistance with data collection.

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

This study was approved by the Joint Chinese University of Hong Kong–New Territories East Cluster Clinical Research Ethics Committee (REC Ref. No.: 2020.232), which waived the requirement for informed consent due to the retrospective nature of the study. The study was conducted in compliance with the established ethical standards and principles of the Declaration of Helsinki.

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