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COVID-19 findings in chest computed tomography

SUMMARY

OBJECTIVE:

The aim of this study was to describe chest computed tomography image findings in patients with COVID-19.

METHODS:

The chest computed tomography scans of 453 hospitalized patients with confirmed COVID-19 were collected at two tertiary care Brazilian hospitals. Demographics and clinical data were extracted from the electronic record medical system.

RESULTS:

The main chest computed tomography findings were ground-glass opacities (92.5%), consolidation (79.2%), crazy-paving pattern (23.9%), parenchymal bands (50%), septal thickening (43.5%), and inverted halo sign (3.5%). Of the 453 hospitalized patients, 136 (30%) died. In this group, ground-glass opacities (94.1%), consolidation (89.7%), septal thickening (58.1%), crazy-paving pattern (52.2%), and parenchymal bands (39.7%) were the most common imaging findings.

CONCLUSIONS:

In a dynamic disease with a broad clinical spectrum such as COVID-19, radiologists can cooperate in a better patient management. On wisely indicated chest computed tomography scans, the fast identification of poor prognosis findings could advise patient management through hospital care facilities and clinical team decisions.

KEYWORDS:
COVID-19; CT x ray; Lung; Thorax; SARS-CoV-2

INTRODUCTION

Being declared by the World Health Organization (WHO) as a pandemic on March 11, 2019, the novel coronavirus disease (COVID-19)11 World Health Organization. WHO Director-General's opening remarks at the media briefing on COVID-19 – 11 March 2020 [internet]. Geneva: World Health Organization; 2020. [cited on Nov. 10, 2020]. Available from: https://www.who.int/director-general/speeches/detail/who-director-general-s-opening-remarks-at-the-media-briefing-on-covid-19–––11-march-2020
https://www.who.int/director-general/spe...
became a major challenge for health care systems worldwide. It was first described on December 2019 as an “unknown etiology pneumonia” at Hubei, a province of China22 Zhu N, Zhang D, Wang W, Li X, Yang B, Song J, et al. A Novel Coronavirus from Patients with Pneumonia in China, 2019. N Engl J Med. 2020;382(8):727-33. https://doi.org/10.1056/NEJMoa2001017
https://doi.org/10.1056/NEJMoa2001017...
. COVID-19 will hallmark human history as one of the most impressive public health calamities: a life-threatening disease steadily increasing the cause of more than 1 million death and 141 million confirmed cases worldwide33 The Johns Hopkins University and medicine. COVID-19 Dashboard by the Center for Systems Science and Engineering (CSSE) at Johns Hopkins University (JHU) [internet]. Baltimore: The Johns Hopkins University and medicine; 2020. [cited on Jan. 29, 2020]. Available from: https://coronavirus.jhu.edu/map.html
https://coronavirus.jhu.edu/map.html...
, not to mention the social, economic, and political distress.

In this scenario, thoracic imaging can be assessed for diagnosis and clinical course monitoring. Although X-rays and ultrasonography have proved their utility, especially on intensive care unit (ICU) and campaign hospitals settings, high-definition computed tomography (HDCT) is the first choice when imaging is required due to its high sensitivity44 Wu G, Li X. Mobile X-rays are highly valuable for critically ill COVID patients. Eur Radiol. 2020;30(9):5217-9. https://doi.org/10.1007/s00330-020-06918-2
https://doi.org/10.1007/s00330-020-06918...
66 Manna S, Wruble J, Maron SZ, Toussie D, Voutsinas N, Finkelstein M, et al. COVID-19: a multimodality review of radiologic techniques, clinical utility, and imaging features. Radiol Cardiothorac Imaging. 2020;2(3):e200210. https://doi.org/10.1148/ryct.2020200210
https://doi.org/10.1148/ryct.2020200210...
. However, the low specificity of the computed tomography (CT)77 Xu B, Xing Y, Peng J, Zheng Z, Tang W, Sun Y, et al. Chest CT for detecting COVID-19: a systematic review and meta-analysis of diagnostic accuracy. Eur Radiol. 2020;30(10):5720-7. https://doi.org/10.1007/s00330-020-06934-2
https://doi.org/10.1007/s00330-020-06934...
explained why radiology societies' recommendations are against the method as an initial approach to diagnosis88 American College of Radiology. ACR recommendations for the use of chest radiography and computed tomography (CT) for suspected COVID-19 infection [internet]. Washington DC: American College of Radiology; 2020. [cited on Oct. 2, 2020]. Available from: https://www.acr.org/Advocacy-and-Economics/ACR-Position-Statements/Recommendations-for-Chest-Radiography-and-CT-for-Suspected-COVID19-Infection
https://www.acr.org/Advocacy-and-Economi...
,99 Colégio Brasileiro de Radiologia e Diagnóstico por Imagem. Recomendações de uso de métodos de imagem para pacientes suspeitos de infecção pelo COVID-19 versão 3 [internet]. São Paulo: Colégio Brasileiro de Radiologia e Diagnóstico por Imagem; 2020 [cited on Sept. 3, 2020]. Available from: https://cbr.org.br/wp-content/uploads/2020/06/Recomendacoes-de-uso-de-metodos-de-imagem-para-pacientes-suspeitos-de-infeccao-pelo-COVID19_v3.pdf
https://cbr.org.br/wp-content/uploads/20...
. Even though reverse transcription polymerase chain reaction (RT-PCR) tests were adopted as the reference standard, dissociation between laboratory and tomographic findings must be expected and CT manifestations remain critical for patient management when first RT-PCR results are negative or unknown1010 Long C, Xu H, Shen Q, Zhang X, Fan B, Wang C, et al. Diagnosis of the Coronavirus disease (COVID-19): rRT-PCR or CT? Eur J Radiol. 2020;126:108961. https://doi.org/10.1016/j.ejrad.2020.108961
https://doi.org/10.1016/j.ejrad.2020.108...
.

To contribute with the current literature, the present study describes chest CT findings in patients with COVID-19 in the Brazilian State of Espírito Santo and correlates the results with in-hospital mortality.

METHODS

A retrospective study was conducted focusing on analyzing thoracic findings in hospitalized patients with SARS-CoV-2 confirmed with real-time reverse transcriptase polymerase chain reaction (rRT-PCR) of respiratory secretions or rapid detection tests to detect the SARS-CoV-2 antibody. It was a multicentric data analysis by two tertiary care Brazilian hospitals, one in Vitória-ES (Hospital Universitário Cassiano Antônio Moraes or HUCAM) and the other one in Serra-ES (Hospital Estadual Jayme Santos Neves or HEJSN).

All imaging examinations were performed according to the clinical indications. CT imaging was performed using Toshiba Alexion 16-slice (Toshiba Medical Systems, Nasu, Japan) at HEJSN and Toshiba 64-slice (Toshiba Medical Systems) at HUCAM. The protocols in both institutions were similar with 2-mm-section thickness, 40 cm field of view, 120 kV (peak), and 200–260 mA. This study was approved by the research ethics committee (CAAE 31424720.1.0000.5071).

Four radiologists (C.C., Y.O., B.B.Z., and W.B. with 1, 3, 3, and 5 years of experience in interpreting CT images, respectively) reviewed the first CT scans of these patients. The radiologists evaluated the initial CT for ground-glass opacities, consolidation, septal thickening, parenchymal bands, inverted halo sign, crazy-paving pattern, lobes affected, pleural effusion, thoracic lymphadenopathy (lymph node size of ≥1 cm in short-axis dimension), and other abnormalities (pneumothorax, pneumomediastinum, bronchiectasis, pulmonary cysts, cavitated nodule, pulmonary emphysema, and random nodules). They classify the degree of lung involvement qualitatively through visual analysis as none (0%), minimal (1–25%), mild (26–50%), moderate (51–75%), or severe (76–100%). Clinical information was collected from the electronic medical records. The analysis of the axial distribution of the lesions was performed, which was classified as lesions with central distribution or lesions with peripheral distribution.

RESULTS

In this study, 453 CTs of hospitalized patients from March to July 2020 were analyzed. The main CT findings were ground-glass opacities in 419 (92.5%) patients, consolidation in 359 (79.2%), crazy-paving pattern in 122 (23.9%), parenchymal bands in 226 (50%), septal thickening in 197 (43.5%), and inverted halo sign in 16 (3.5%) patients. Pleural effusion was found in 83 (18.3%) patients and lymph node enlargement in 26 (5.7%), as given in Table 1.

Table 1
Demographics and CT characteristics.

We observed severe pulmonary involvement in 59 (13%) patients, moderate involvement in 145 (32%), mild involvement in 135 (29.8%), minimal involvement in 95 (21%), and 19 (4.2%) with none pulmonary involvement. The qualitative visual assessment of each one of the pulmonary lobes revealed a predominance of greater involvement in the lower lobes. Most patients had a bilateral multilobar pattern of involvement, with only nine patients with unilobar commitment.

Out of 453, 136 (30%) patients died during hospitalization. Of these, the distribution of the findings occurred as follows: ground-glass opacities in 128 (94.1%) patients, consolidation in 122 (89.7%), crazy-paving pattern in 71 (52.2%), septal thickening in 79 (58.1%), parenchymal bands in 54 (39.7%), and inverted halo sign in three (2.2%). Pleural effusion was found in 29 (21.3%) patients, being the sole observation in one of them (0.7%). Lymph node enlargement was identified in 12 (8.8%) individuals who died and 5 (3.7%) had normal initial CT. Pneumomediastinum was found in six patients, five of whom died (Figures 1 and 2).

Figure 1
(A) Opacities with ground-glass attenuation (arrow). (B) Diffuse consolidation (arrows).
Figure 2
(A) Reticular opacities and ground-glass attenuation (arrow). (B) Ground-glass attenuation opacities surrounded by a consolidation ring – the reversed halo sign (arrow).

Of the patients who died, 13 (9.6%) had minimal pulmonary involvement, 25 (18.4%) had mild involvement, 53 (39%) had moderate involvement, and 40 (29.4%) had severe involvement.

DISCUSSION

The pulmonary pathogenesis caused by SARS-CoV-2 has been associated with the coronavirus entrance in cells through angiotensin-converting enzyme two receptor, abundant on the acinar side of pneumocytes within alveolar spaces. Once tissues are perpetrated, immune and nonimmune cells promote cytokines storm, resulting in damage to the host1111 Revzin MV, Raza S, Warshawsky R, D’Agostino C, Srivastava NC, Bader AS, et al. Multisystem imaging manifestations of COVID-19, part 1: viral pathogenesis and pulmonary and vascular system complications. Radiographics. 2020;40(6):1574-99. https://doi.org/10.1148/rg.2020200149
https://doi.org/10.1148/rg.2020200149...
. Fever and respiratory symptoms are the most common manifestations, as expected for an infectious pulmonary disease. Clinical findings can be diverse, ranging from asymptomatic patients to critical disease, and from sole lung impairment to multisystemic presentations1111 Revzin MV, Raza S, Warshawsky R, D’Agostino C, Srivastava NC, Bader AS, et al. Multisystem imaging manifestations of COVID-19, part 1: viral pathogenesis and pulmonary and vascular system complications. Radiographics. 2020;40(6):1574-99. https://doi.org/10.1148/rg.2020200149
https://doi.org/10.1148/rg.2020200149...
,1212 Gandhi RT, Lynch JB, Del Rio C. Mild or moderate Covid-19. N Engl J Med. 2020;383(18):1757-66. https://doi.org/10.1056/NEJMcp2009249
https://doi.org/10.1056/NEJMcp2009249...
.

Although mild and moderate presentations are preponderant, COVID-19 is a dynamic disease with a quick clinical deterioration among severe symptomatic individuals, a group with considerable risk of prolonged critical illness and death1313 Berlin DA, Gulick RM, Martinez FJ. Severe Covid-19. N Engl J Med. 2020;383(25):2451-60. https://doi.org/10.1056/NEJMcp2009575
https://doi.org/10.1056/NEJMcp2009575...
. Mortality among hospitalized patients in ICUs varies from 30% to 70% in the literature1414 Martins-Filho PR, Tavares CSS, Santos VS. Factors associated with mortality in patients with COVID-19. A quantitative evidence synthesis of clinical and laboratory data. Eur J Intern Med. 2020;76:97-9. https://doi.org/10.1016/j.ejim.2020.04.043
https://doi.org/10.1016/j.ejim.2020.04.0...
. Similarly, we found 30% mortality in our patients, with the most important findings related to mortality: age over 60 years, female, and moderate or severe pulmonary involvement. To avoid unwanted outcomes, physicians must identify the main factors of poor prognosis, making quicker decisions and setting appropriate treatment goals1313 Berlin DA, Gulick RM, Martinez FJ. Severe Covid-19. N Engl J Med. 2020;383(25):2451-60. https://doi.org/10.1056/NEJMcp2009575
https://doi.org/10.1056/NEJMcp2009575...
. An extent of different scenarios must be considered while interpreting deaths, from the environmental factors to the therapeutic limitations. In addition to this complexity, the results of the present study have important practical implications, providing indicators related to the increased risk of death from COVID-19 and meaningful on guiding physicians' decisions about intensive care practices in ICU settings1414 Martins-Filho PR, Tavares CSS, Santos VS. Factors associated with mortality in patients with COVID-19. A quantitative evidence synthesis of clinical and laboratory data. Eur J Intern Med. 2020;76:97-9. https://doi.org/10.1016/j.ejim.2020.04.043
https://doi.org/10.1016/j.ejim.2020.04.0...
.

Qualitative visual assessment of pulmonary involvement is a metric worth attention. In this study, most of the hospitalized patients had a pulmonary involvement more than 25% and the majority of the patients who died had pulmonary involvement more than 50%, inferring a worse prognosis related to the size of the affected area. Toussie et al.1515 Toussie D, Voutsinas N, Finkelstein M, Cedillo MA, Manna S, Maron SZ, et al. Clinical and Chest Radiography Features Determine Patient Outcomes in Young and Middle-aged Adults with COVID-19 Radiology. 2020;297(1):E197-206. https://doi.org/10.1148/radiol.2020201754
https://doi.org/10.1148/radiol.202020175...
reported that patients with ground-glass opacities represented in at least two pulmonary zones are more likely to need hospitalization and those in three zones were more likely to intubate, reinforcing the prerogative that the largest area affected is related to worse prognosis.

The main CT findings are similar to those that have been described in the literature, including predominantly bilateral multifocal ground-glass opacities, sometimes associated with a superimposed thin septal thickening (“crazy-paving” pattern), usually involving several pulmonary lobes and with distribution predominantly peripheral in the parenchyma1616 Barbosa PNVP, Bitencourt AGV, de Miranda GD, Almeida MFA, Chojniak R. Chest CT accuracy in the diagnosis of SARS-CoV-2 infection: initial experience in a cancer center. Radiol Bras. 2020;53(4):211-5. https://doi.org/10.1590/0100-3984.2020.0040
https://doi.org/10.1590/0100-3984.2020.0...
,1717 Carotti M, Salaffi F, Sarzi-Puttini P, Agostini A, Borgheresi A, Minorati D, et al. Chest CT features of coronavirus disease 2019 (COVID-19) pneumonia: key points for radiologists. Radiol Med. 2020;125(7):636-46. https://doi.org/10.1007/s11547-020-01237-4
https://doi.org/10.1007/s11547-020-01237...
.

Pulmonary cavitation and pneumothorax are less common findings in COVID-19 and, when described, should raise suspicion for other potential causes1111 Revzin MV, Raza S, Warshawsky R, D’Agostino C, Srivastava NC, Bader AS, et al. Multisystem imaging manifestations of COVID-19, part 1: viral pathogenesis and pulmonary and vascular system complications. Radiographics. 2020;40(6):1574-99. https://doi.org/10.1148/rg.2020200149
https://doi.org/10.1148/rg.2020200149...
. The low incidence of pleural effusion and the absence of other findings, such as lymph node enlargement, nodules, and excavated lesions, are in line with recent international experience1818 Chate RC, Fonseca EKUN, Passos RBD, Teles GBDS, Shoji H, Szarf G. Presentation of pulmonary infection on CT in COVID-19: initial experience in Brazil. J Bras Pneumol. 2020;46(2):e20200121. https://doi.org/10.36416/1806-3756/e20200121
https://doi.org/10.36416/1806-3756/e2020...
. Unilateral lesions are also uncommon, described only in 2% of patients with COVID-19 in the literature, and may be useful in differentiating COVID-19 pneumonia from other conditions1111 Revzin MV, Raza S, Warshawsky R, D’Agostino C, Srivastava NC, Bader AS, et al. Multisystem imaging manifestations of COVID-19, part 1: viral pathogenesis and pulmonary and vascular system complications. Radiographics. 2020;40(6):1574-99. https://doi.org/10.1148/rg.2020200149
https://doi.org/10.1148/rg.2020200149...
.

It is important to recognize that imaging findings of the new coronavirus share some similarities with other diseases that cause viral pneumonia, particularly those within the same viral family (SARS and MERS). As new cases are identified, other exclusive pulmonary manifestations may emerge as potential points for discernment in this patient population. Future research studies will be essential to determine how patients with parenchymal lung disease evolve after the treatment1919 Ai T, Yang Z, Hou H, Zhan C, Chen C, Lv W, et al. Correlation of chest CT and RT-PCR testing for Coronavirus disease 2019 (COVID-19) in China: a report of 1014 cases. Radiology. 2020;296(2):E32-40. https://doi.org/10.1148/radiol.2020200642
https://doi.org/10.1148/radiol.202020064...
. Vidal et al.2020 Garcia-Vidal C, Sanjuan G, Moreno-García E, Puerta-Alcalde P, Garcia-Pouton N, Chumbita M, et al. Incidence of co-infections and superinfections in hospitalized patients with COVID-19: a retrospective cohort study. Clin Microbiol Infect. 2021;27(1):83-8. https://doi.org/10.1016/j.cmi.2020.07.041
https://doi.org/10.1016/j.cmi.2020.07.04...
reported that bacterial, fungal, and viral coinfections and superinfections in patients hospitalized with COVID-19 are low; however, when present, they can cause serious diseases. Therefore, any unusual finding may lead to further investigation.

A limitation of our study is the lack of data on patients' comorbidities; however, Revsing et al.1111 Revzin MV, Raza S, Warshawsky R, D’Agostino C, Srivastava NC, Bader AS, et al. Multisystem imaging manifestations of COVID-19, part 1: viral pathogenesis and pulmonary and vascular system complications. Radiographics. 2020;40(6):1574-99. https://doi.org/10.1148/rg.2020200149
https://doi.org/10.1148/rg.2020200149...
reported an increased risk of developing severe disease and increased mortality in patients with underlying cardiovascular disease, diabetes mellitus, hypertension, chronic lung disease, cancer (particularly hematological malignancies, lung cancer, and metastatic disease), obesity, and chronic kidney disease. The Centers for Disease Control and Prevention also includes immunocompromised status and liver disease as potential risk factors for serious illnesses, although specific data on the risks associated with these conditions are limited1111 Revzin MV, Raza S, Warshawsky R, D’Agostino C, Srivastava NC, Bader AS, et al. Multisystem imaging manifestations of COVID-19, part 1: viral pathogenesis and pulmonary and vascular system complications. Radiographics. 2020;40(6):1574-99. https://doi.org/10.1148/rg.2020200149
https://doi.org/10.1148/rg.2020200149...
,2121 Zhou J, Huang L, Chen J, Yuan X, Shen Q, Dong S, et al. Clinical features predicting mortality risk in older patients with COVID-19. Curr Med Res Opin. 2020;36(11):1753-9. https://doi.org/10.1080/03007995.2020.1825365
https://doi.org/10.1080/03007995.2020.18...
.

Chest radiography is generally the initial imaging method and the American College of Radiology advises against the use of CT as a first-line tool in the diagnosis of COVID-19, recommending it to be used in moderation and reserved for symptomatic patients hospitalized with specific clinical indications, as an assessment of complications1111 Revzin MV, Raza S, Warshawsky R, D’Agostino C, Srivastava NC, Bader AS, et al. Multisystem imaging manifestations of COVID-19, part 1: viral pathogenesis and pulmonary and vascular system complications. Radiographics. 2020;40(6):1574-99. https://doi.org/10.1148/rg.2020200149
https://doi.org/10.1148/rg.2020200149...
. However, Tao et al.2222 Guan W, Ni Z, Hu Y, Liang WH, Ou CQ, He JX, et al. Clinical characteristics of Coronavirus Disease 2019 in China. N Engl J Med. 2020;382(18):1708-20. https://doi.org/10.1056/NEJMoa2002032
https://doi.org/10.1056/NEJMoa2002032...
reported that 97% of patients confirmed with COVID-19 with RT-PCR assays had positive results on chest CT, confirming a high sensitivity in detecting the disease.

CONCLUSIONS

This work represents an investigation of the chest CT findings in hospitalized patients with COVID-19. The radiologist plays a crucial role in the fast identification and early diagnosis of new cases, in addition to identifying factors of worse prognosis, which can be a great benefit not only for the patient but also for the broader health surveillance and response systems public2323 Chung M, Bernheim A, Mei X, Zhang N, Huang M, Zeng X, et al. CT imaging features of 2019 novel Coronavirus (2019-nCoV). Radiology. 2020;295(1):202-7. https://doi.org/10.1148/radiol.2020200230
https://doi.org/10.1148/radiol.202020023...
. Therefore, the CT evaluation, when well indicated, offers important information, identifying typical findings or suggesting other diagnoses and findings about a worse prognosis, unfavorable evolution, or mortality, such as consolidation or crazy-paving pattern, pneumomediastinum, and moderate/severe pulmonary involvement.

  • Funding: this work was supported by the State Hospital Jayme Santos Neves linked to the State Secretary of Health of Espírito Santo (Sesa/ES), Brazil. Fernanda Filetti Ferreira was supported by the Fundação de Amparo à Pesquisa e Inovação do Espírito Santo FAPES.

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    Barbosa PNVP, Bitencourt AGV, de Miranda GD, Almeida MFA, Chojniak R. Chest CT accuracy in the diagnosis of SARS-CoV-2 infection: initial experience in a cancer center. Radiol Bras. 2020;53(4):211-5. https://doi.org/10.1590/0100-3984.2020.0040
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    » https://doi.org/10.1007/s11547-020-01237-4
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    Chate RC, Fonseca EKUN, Passos RBD, Teles GBDS, Shoji H, Szarf G. Presentation of pulmonary infection on CT in COVID-19: initial experience in Brazil. J Bras Pneumol. 2020;46(2):e20200121. https://doi.org/10.36416/1806-3756/e20200121
    » https://doi.org/10.36416/1806-3756/e20200121
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Publication Dates

  • Publication in this collection
    26 Nov 2021
  • Date of issue
    Oct 2021

History

  • Received
    13 July 2021
  • Accepted
    16 Aug 2021
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