COVID-19 pneumonia on chest X-rays: Performance of a deep learning-based computer-aided detection system

Eui Jin Hwang, Ki Beom Kim, Jin Young Kim, Jae-Kwang Lim, Ju Gang Nam, Hyewon Choi, Hyungjin Kim, Soon Ho Yoon, Jin Mo Goo, Chang Min Park, Eui Jin Hwang, Ki Beom Kim, Jin Young Kim, Jae-Kwang Lim, Ju Gang Nam, Hyewon Choi, Hyungjin Kim, Soon Ho Yoon, Jin Mo Goo, Chang Min Park

Abstract

Chest X-rays (CXRs) can help triage for Coronavirus disease (COVID-19) patients in resource-constrained environments, and a computer-aided detection system (CAD) that can identify pneumonia on CXR may help the triage of patients in those environment where expert radiologists are not available. However, the performance of existing CAD for identifying COVID-19 and associated pneumonia on CXRs has been scarcely investigated. In this study, CXRs of patients with and without COVID-19 confirmed by reverse transcriptase polymerase chain reaction (RT-PCR) were retrospectively collected from four and one institution, respectively, and a commercialized, regulatory-approved CAD that can identify various abnormalities including pneumonia was used to analyze each CXR. Performance of the CAD was evaluated using area under the receiver operating characteristic curves (AUCs), with reference standards of the RT-PCR results and the presence of findings of pneumonia on chest CTs obtained within 24 hours from the CXR. For comparison, 5 thoracic radiologists and 5 non-radiologist physicians independently interpreted the CXRs. Afterward, they re-interpreted the CXRs with corresponding CAD results. The performance of CAD (AUCs, 0.714 and 0.790 against RT-PCR and chest CT, respectively hereinafter) were similar with those of thoracic radiologists (AUCs, 0.701 and 0.784), and higher than those of non-radiologist physicians (AUCs, 0.584 and 0.650). Non-radiologist physicians showed significantly improved performance when assisted with the CAD (AUCs, 0.584 to 0.664 and 0.650 to 0.738). In addition, inter-reader agreement among physicians was also improved in the CAD-assisted interpretation (Fleiss' kappa coefficient, 0.209 to 0.322). In conclusion, radiologist-level performance of the CAD in identifying COVID-19 and associated pneumonia on CXR and enhanced performance of non-radiologist physicians with the CAD assistance suggest that the CAD can support physicians in interpreting CXRs and helping image-based triage of COVID-19 patients in resource-constrained environment.

Conflict of interest statement

I have read the journal’s policy and the authors of this manuscript have the following competing interests: Chang Min Park holds stock of Promedius and stock options of Lunit Inc. and Coreline Soft. Eui Jin Hwang, Hyungjin Kim, and Chang Min Park received research grants from Lunit Inc, outside the present paper. We checked all authors’ competing interests and confirmed that our statement does not alter the adherence to PLOS ONE policy.

Figures

Fig 1. Flow diagram for patients’ inclusion.
Fig 1. Flow diagram for patients’ inclusion.
A total of 80 patients with COVID-19 were retrospectively included from four institutions, while 92 patients without COVID-19 were included from single institution. Among patients with COVID-19, 67 exhibited findings of pneumonia on chest CT obtained within 24 hours from CXR, while the other 13 patients did not exhibited any findings of pneumonia on chest CT.
Fig 2. Representative case with COVID-19 pneumonia.
Fig 2. Representative case with COVID-19 pneumonia.
A CXR (A) of a patient with confirmed COVID-19 shows patchy infiltrates in both lower lung fields (arrows). The corresponding chest CT image (B) obtained in the same day with the CXR shows multifocal patchy ground-glass opacities in both lower lobes of the lung. The CT severity score of the patient was 13. The CAD system correctly detected pulmonary infiltrates with a probability score of 56% (C). In the reader-alone interpretation, four thoracic radiologists correctly identified the abnormality while none of the non-radiologist physicians identified the abnormality. In the CAD-assisted interpretation, all five thoracic radiologists and four non-radiologist physicians identified the abnormality.
Fig 3. Representative case without COVID-19 pneumonia.
Fig 3. Representative case without COVID-19 pneumonia.
A CXR (A) and corresponding chest CT (B) of a patient with fever and dyspnea but negative RT-PCR result for COVID-19 show no pulmonary abnormality suggestive of pneumonia. The CAD system did not detect any abnormalities in the CXR and the probability score was 13% (C). In the reader-alone interpretation, four thoracic radiologists and four non-radiologist physicians misclassified the CXR as having findings of pneumonia. In the CAD-assisted interpretation, only one thoracic radiologist and two non-radiologist physicians made false-positive classification of the CXR. Mediastinal window CT image (D) show pulmonary embolism in the right descending pulmonary artery (arrow), presumed cause of patients’ symptom.
Fig 4. Performance of the CAD versus…
Fig 4. Performance of the CAD versus reader-alone interpretations.
For identification of RT-PCR-positive COVID-19 patients (A), the CAD exhibited AUC of 0.714 (black line), which did not significantly differ from that of thoracic radiologists (0.701, blue line) but significantly higher than that of non-radiologist physicians (0.584, red line). For identification of pneumonia defined on chest CT (B), the CAD exhibited AUC of 0.790 (black line), which was not significantly different from that of thoracic radiologists (0.784, blue line), but significantly higher than that of non-radiologist physicians (0.650, red line).
Fig 5. Performance of physician alone versus…
Fig 5. Performance of physician alone versus CAD-assisted interpretations.
For identification of RT-PCR positive COVID-19 patients, the AUCs of thoracic radiologists did not significantly differ between reader-alone (red line) and CAD-assisted interpretations (blue line) (0.701 vs. 0.699; P = .815) (A), while the AUC non-radiologist physicians was significantly improved in the CAD-assisted interpretation (blue line) compared to the reader-alone interpretation (red line) (0.584 vs. 0.664; P = .006) (B). For identification of pneumonia defined on chest CT, the AUCs of thoracic radiologists also did not significantly differ between reader-alone (red line) and CAD-assisted interpretations (blue line) (0.784 vs. 0.789; P = .524) (C), while the AUC non-radiologist physicians was significantly improved in the CAD-assisted interpretation (blue line) compared to the reader-alone interpretation (red line) (0.650 vs. 0.738; P = .003) (D).

References

    1. World Health Organization. Weekly epidemiological update on COVID-19–30 March 2021 March 30, 2021 [cited 2021 April 12]. Available from: .
    1. Guan WJ, Ni ZY, 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. Epub 2020/02/29. doi: 10.1056/NEJMoa2002032 ; PubMed Central PMCID: PMC7092819.
    1. Sakurai A, Sasaki T, Kato S, Hayashi M, Tsuzuki SI, Ishihara T, et al.. Natural History of Asymptomatic SARS-CoV-2 Infection. N Engl J Med. 2020;383(9):885–6. Epub 2020/06/13. doi: 10.1056/NEJMc2013020 ; PubMed Central PMCID: PMC7304419.
    1. Rothe C, Schunk M, Sothmann P, Bretzel G, Froeschl G, Wallrauch C, et al.. Transmission of 2019-nCoV Infection from an Asymptomatic Contact in Germany. N Engl J Med. 2020;382(10):970–1. Epub 2020/02/01. doi: 10.1056/NEJMc2001468 ; PubMed Central PMCID: PMC7120970.
    1. Hellewell J, Abbott S, Gimma A, Bosse NI, Jarvis CI, Russell TW, et al.. Feasibility of controlling COVID-19 outbreaks by isolation of cases and contacts. Lancet Glob Health. 2020;8(4):e488–e96. Epub 2020/03/03. doi: 10.1016/S2214-109X(20)30074-7 ; PubMed Central PMCID: PMC7097845.
    1. World Health Organization. Laboratory testing for coronavirus disease 2019 (COVID-19) in suspected human cases March 2, 2020 [cited 2020 May 15]. Available from: .
    1. Unites States Centers for Disease Control and Prevention USCfDCa. Interim Guidelines for Collecting, Handling, and Testing Clinical Specimens from Persons for Coronavirus Disease 2019 (COVID-19) February 14, 2020 [cited 2020 March 18]. Available from: .
    1. Yoon SH, Lee KH, Kim JY, Lee YK, Ko H, Kim KH, et al.. Chest Radiographic and CT Findings of the 2019 Novel Coronavirus Disease (COVID-19): Analysis of Nine Patients Treated in Korea. Korean J Radiol. 2020. Epub 2020/02/27. doi: 10.3348/kjr.2020.0132 .
    1. Bernheim A, Mei X, Huang M, Yang Y, Fayad ZA, Zhang N, et al.. Chest CT Findings in Coronavirus Disease-19 (COVID-19): Relationship to Duration of Infection. Radiology. 2020:200463. Epub 2020/02/23. doi: 10.1148/radiol.2020200463 .
    1. Chung M, Bernheim A, Mei X, Zhang N, Huang M, Zeng X, et al.. CT Imaging Features of 2019 Novel Coronavirus (2019-nCoV). Radiology. 2020:200230. Epub 2020/02/06. doi: 10.1148/radiol.2020200230 .
    1. Rubin GD, Ryerson CJ, Haramati LB, Sverzellati N, Kanne JP, Raoof S, et al.. The Role of Chest Imaging in Patient Management during the COVID-19 Pandemic: A Multinational Consensus Statement from the Fleischner Society. Radiology. 2020:201365. Epub 2020/04/08. doi: 10.1148/radiol.2020201365 .
    1. Foust AM, Phillips GS, Chu WC, Daltro P, Das KM, Garcia-Peña P, et al.. International Expert Consensus Statement on Chest Imaging in Pediatric COVID-19 Patient Management: Imaging Findings, Imaging Study Reporting and Imaging Study Recommendations. Radiology: Cardiothoracic Imaging. 2020;2(2):e200214. doi: 10.1148/ryct.2020200214
    1. American College of Radiology. ACR Recommendations for the use of Chest Radiography and Computed Tomography (CT) for Suspected COVID-19 Infection March 11, 2020 [cited 2020 March 18]. Available from: .
    1. Society of Thoracic Radiology. STR/ASER COVID-19 Position Statement March 11, 2020 [cited 2020 Marh 20]. Available from: .
    1. Emanuel EJ, Persad G, Upshur R, Thome B, Parker M, Glickman A, et al.. Fair Allocation of Scarce Medical Resources in the Time of Covid-19. N Engl J Med. 2020;382(21):2049–55. Epub 2020/03/24. doi: 10.1056/NEJMsb2005114 .
    1. American Society for Microbiology. Supply shortages impacting COVID-19 and non-COVID testing. 2020. Available from: .
    1. Ranney ML, Griffeth V, Jha AK. Critical Supply Shortages—The Need for Ventilators and Personal Protective Equipment during the Covid-19 Pandemic. N Engl J Med. 2020;382(18):e41. Epub 2020/03/27. doi: 10.1056/NEJMp2006141 .
    1. Wong HYF, Lam HYS, Fong AH, Leung ST, Chin TW, Lo CSY, et al.. Frequency and Distribution of Chest Radiographic Findings in COVID-19 Positive Patients. Radiology. 2019:201160. Epub 2020/03/29. doi: 10.1148/radiol.2020201160 .
    1. Choi H, Qi X, Yoon SH, Park SJ, Lee KH, Kim JY, et al.. Extension of coronavirus disease 2019 (COVID-19) on chest CT and implications for chest radiograph interpretation. Radiology: Cardiothoracic Imaging. 2020;2(2):e200107. doi: 10.1148/ryct.2020200107
    1. Orsi MA, Oliva AG, Cellina M. Radiology Department Preparedness for COVID-19: Facing an Unexpected Outbreak of the Disease. Radiology. 2020:201214. Epub 2020/04/02. doi: 10.1148/radiol.2020201214 .
    1. Hwang EJ, Park S, Jin KN, Kim JI, Choi SY, Lee JH, et al.. Development and Validation of a Deep Learning-Based Automated Detection Algorithm for Major Thoracic Diseases on Chest Radiographs. JAMA Netw Open. 2019;2(3):e191095. Epub 2019/03/23. doi: 10.1001/jamanetworkopen.2019.1095 ; PubMed Central PMCID: PMC6583308.
    1. Park S, Lee SM, Lee KH, Jung KH, Bae W, Choe J, et al.. Deep learning-based detection system for multiclass lesions on chest radiographs: comparison with observer readings. Eur Radiol. 2020;30(3):1359–68. Epub 2019/11/22. doi: 10.1007/s00330-019-06532-x .
    1. Nam JG, Park S, Hwang EJ, Lee JH, Jin KN, Lim KY, et al.. Development and Validation of Deep Learning-based Automatic Detection Algorithm for Malignant Pulmonary Nodules on Chest Radiographs. Radiology. 2019;290(1):218–28. Epub 2018/09/27. doi: 10.1148/radiol.2018180237 .
    1. Majkowska A, Mittal S, Steiner DF, Reicher JJ, McKinney SM, Duggan GE, et al.. Chest Radiograph Interpretation with Deep Learning Models: Assessment with Radiologist-adjudicated Reference Standards and Population-adjusted Evaluation. Radiology. 2020;294(2):421–31. Epub 2019/12/04. doi: 10.1148/radiol.2019191293 .
    1. Hwang EJ, Nam JG, Lim WH, Park SJ, Jeong YS, Kang JH, et al.. Deep Learning for Chest Radiograph Diagnosis in the Emergency Department. Radiology. 2019;293(3):573–80. Epub 2019/10/23. doi: 10.1148/radiol.2019191225 .
    1. Annarumma M, Withey SJ, Bakewell RJ, Pesce E, Goh V, Montana G. Automated Triaging of Adult Chest Radiographs with Deep Artificial Neural Networks. Radiology. 2019;291(1):196–202. Epub 2019/01/23. doi: 10.1148/radiol.2018180921 ; PubMed Central PMCID: PMC6438359.
    1. Murphy K, Smits H, Knoops AJG, Korst M, Samson T, Scholten ET, et al.. COVID-19 on the Chest Radiograph: A Multi-Reader Evaluation of an AI System. Radiology. 2020:201874. Epub 2020/05/10. doi: 10.1148/radiol.2020201874 .
    1. Wehbe RM, Sheng J, Dutta S, Chai S, Dravid A, Barutcu S, et al.. DeepCOVID-XR: An Artificial Intelligence Algorithm to Detect COVID-19 on Chest Radiographs Trained and Tested on a Large US Clinical Dataset. Radiology. 2020:203511. Epub 2020/11/25. doi: 10.1148/radiol.2020203511 .
    1. Hwang EJ, Kim H, Yoon SH, Goo JM, Park CM. Implementation of a Deep Learning-Based Computer-Aided Detection System for the Interpretation of Chest Radiographs in Patients Suspected for COVID-19. Korean J Radiol. 2020;21(10):1150–60. Epub 2020/07/31. doi: 10.3348/kjr.2020.0536 ; PubMed Central PMCID: PMC7458860.
    1. Yang R, Li X, Liu H, Zhen Y, Zhang X, Xiong Q, et al.. Chest ct severity score: An imaging tool for assessing severe covid-19. Radiology: Cardiothoracic Imaging. 2020;2(2):e200047. doi: 10.1148/ryct.2020200047
    1. Obuchowski NA Jr, Rockette HE Jr. Hypothesis testing of diagnostic accuracy for multiple readers and multiple tests an anova approach with dependent observations. Communications in Statistics-simulation and Computation. 1995;24(2):285–308.
    1. He JL, Luo L, Luo ZD, Lyu JX, Ng MY, Shen XP, et al.. Diagnostic performance between CT and initial real-time RT-PCR for clinically suspected 2019 coronavirus disease (COVID-19) patients outside Wuhan, China. Respir Med. 2020;168:105980. Epub 2020/05/05. doi: 10.1016/j.rmed.2020.105980 ; PubMed Central PMCID: PMC7172864.
    1. Yang W, Yan F. Patients with RT-PCR-confirmed COVID-19 and Normal Chest CT. Radiology. 2020;295(2):E3. Epub 2020/03/07. doi: 10.1148/radiol.2020200702 .
    1. Xie X, Zhong Z, Zhao W, Zheng C, Wang F, Liu J. Chest CT for Typical 2019-nCoV Pneumonia: Relationship to Negative RT-PCR Testing. Radiology. 2020:200343. Epub 2020/02/13. doi: 10.1148/radiol.2020200343 .
    1. Fang Y, Zhang H, Xie J, Lin M, Ying L, Pang P, et al.. Sensitivity of Chest CT for COVID-19: Comparison to RT-PCR. Radiology. 2020:200432. Epub 2020/02/20. doi: 10.1148/radiol.2020200432 .
    1. Ai T, Yang Z, Hou H, Zhan C, Chen C, Lv W, et al.. Correlation of Chest CT and RT-PCR Testing in Coronavirus Disease 2019 (COVID-19) in China: A Report of 1014 Cases. Radiology. 2020:200642. Epub 2020/02/27. doi: 10.1148/radiol.2020200642 .
    1. Zhao W, Zhong Z, Xie X, Yu Q, Liu J. Relation Between Chest CT Findings and Clinical Conditions of Coronavirus Disease (COVID-19) Pneumonia: A Multicenter Study. AJR Am J Roentgenol. 2020:1–6. Epub 2020/03/04. doi: 10.2214/AJR.20.22976 .
    1. 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 Age Adults with COVID-19. Radiology. 2020:201754. Epub 2020/05/15. doi: 10.1148/radiol.2020201754 .
    1. Shi H, Han X, Jiang N, Cao Y, Alwalid O, Gu J, et al.. Radiological findings from 81 patients with COVID-19 pneumonia in Wuhan, China: a descriptive study. Lancet Infect Dis. 2020. Epub 2020/02/28. doi: 10.1016/S1473-3099(20)30086-4 .
    1. Castiglioni I, Ippolito D, Interlenghi M, Monti CB, Salvatore C, Schiaffino S, et al.. Machine learning applied on chest x-ray can aid in the diagnosis of COVID-19: a first experience from Lombardy, Italy. Eur Radiol Exp. 2021;5(1):7. Epub 2021/02/03. doi: 10.1186/s41747-020-00203-z ; PubMed Central PMCID: PMC7850902.
    1. Minaee S, Kafieh R, Sonka M, Yazdani S, Jamalipour Soufi G. Deep-COVID: Predicting COVID-19 from chest X-ray images using deep transfer learning. Med Image Anal. 2020;65:101794. Epub 2020/08/12. doi: 10.1016/j.media.2020.101794 ; PubMed Central PMCID: PMC7372265.

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