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Case report

Pleural effusion in a COVID-19 patient

Jelena Aritonović Pribaković1,4, Milica Perić2, Jelena Milošević3, Aleksandra Janićević4
  • University of Priština-Kosovska Mitrovica, Faculty of Medicine, Kosovska Mitrovica, Serbia
  • Medical Vocational School, Priština, Gračanica, Serbia
  • Medical Center "Zvezdara", Belgrade, Serbia
  • Medical Center "Priština – Gračanica", Serbia

ABSTRACT

Introduction/Aim: Pleural effusions are rarely seen on computerized tomography (CT) or radiography (X-ray) images of the chest, in coronavirus disease of 2019 (COVID-19). When present, they usually occur late in the course of the disease; they are mostly unilateral but can also be bilateral, and are absorbed after two days. Studies have also shown that pleural effusions occur primarily in the elderly and individuals with underlying respiratory disease. The incidence of respiratory failure and acute respiratory distress syndrome, as well as the mortality rates are higher in patients with pleural effusion than in patients without it. Our aim is to report a case that is different from the most commonly described cases in available literature.

Patient presentation: We present a 49-year-old, comorbidity-free COVID-19 patient, who developed pleural effusion on the 10th day of hospitalization. The pleural effusion was unilateral and did not appear on a repeat lung radiography after four days. Except an elevated platelet count, the blood count parameters were in the reference ranges, while the value of CRP was slightly elevated. The patient was discharged with a good general health status, after 16 days of hospitalization.

Conclusion: This case provides insight into the course and prognosis of the COVID-19 disease that is different from what has been reported in previously published papers and shows that pleural effusions do not occur only in elderly patients with comorbidities and a severe clinical presentation of the COVID-19 infection.


INTRODUCTION

As the global pandemic of the coronavirus disease of 2019 (COVID-19) progresses, many medical specialties still have a key role in establishing diagnosis and treatment. In radiology, most of the literature is focused on computerized tomography (CT) findings of COVID-19 manifestations in the chest [1],[2]. However, due to infection control, which relates to the transportation of patients and decontamination, and because in different parts of the world there is a lack of availability of CT imaging, the chest X-ray, i.e., radiography (RTG) is most commonly used for the identification and monitoring of pulmonary lesions. The American Radiology College (ACR) states that the necessary decontamination of CT machines, after they are used for scanning COVID-19 patients, may negatively affect the availability of radiological diagnostics and suggests the possibility of applying mobile X-rays, thereby minimizing the risk of cross infection [3]. Furthermore, in cases of significant clinical suspicion of COVID-19, a positive RTG finding may render the CT scan unnecessary. Also, application of RTG for early detection of the disease may play an important role in those parts of the world where access to reliable polymerase chain reaction (PCR) testing for COVID-19 is limited [4]. The most common X-ray and CT findings include ground glass opacity with consolidations [4],[5]. Pleural effusion is rarely found on CT and X-ray images of COVID-19 patients, and when they are registered, it is most commonly in the later course of the disease [6],[7],[8]. Pleural effusions are mostly unilateral [9], but may be bilateral, and are absorbed after two days of monitoring [10].

As this is a rare finding in COVID-19, based only on pleural effusion, and without a finding of pulmonary lesions, the correct diagnosis may not be established. Also, studies have shown that the incidence of respiratory insufficiency and the incidence of acute respiratory distress syndrome, as well as the mortality rate, are higher in patients with pleural effusion than in patients without pleural effusion [11].

We present the case of a PCR-confirmed COVID-19 patient, out of a total of 331 patients hospitalized in the period October – December 2020, at the Clinic for Infectious Diseases of the Medical Center Priština - Gračanica, where pleural infusion developed during the course of the disease, but which is different from the cases of pleural effusion most commonly described so far.

CASE REPORT

A 49-year-old female patient was hospitalized on the 7th day of the onset of symptoms, due to persistent elevated body temperature of approximately 38.6 °C, dry cough, malaise and weakness, and pain in the muscles and joints. The patient was previously healthy, without comorbidities and without allergies to medication. She did not smoke nor drink alcohol. At admission, the patient was conscious, oriented, afebrile, with the following vitals: SpO2 89.0%, TA 110/70mmHg. Superficial lymph nodes were not palpable, the clinical presentation of the tonsils and pharynx was normal. Auscultation of the lungs, basally on the right, revealed fine crackles. The abdomen was soft and was not tender on palpation, the liver and spleen were not palpable below the costal margins. There was no edema in the lower extremities. The neurological finding was normal.

The laboratory test results were as follows: RBC 4.25...5.02 (reference range: 3.7 – 5.8 x 1012/L); WBC 4.73...5.5 (reference range: 4 - 10 x 109 /L); ANC 0.55...0.75 (reference range: 0.50 – 0.75); Lymphs 0.41...0.22 (reference range: 0.20 – 0.40); Mo 0.04...0.02 (reference range: 0.02 – 0.10); PLT 171...480...563 (reference range: 150 - 350 x 109 /L); CRP 6...18...30...12 (reference range: < 6 IU/ml); TP 72...67...77 (reference range: 65 - 87 g/L); Alb 45...35...38 (reference range: 38 - 51 g/L), ALT 19...61...46 (reference range: <32 U/L); AST 34...87...29 (reference range: < 31 U/L); ALP 89...95...88 (reference range: 64 - 306 U/L); LDH 473...721...419 (reference range: 225 - 450 U/L); CK 209...89...29 (reference range: 24 - 170 U/L). The PCR test showed that the patient was positive for SARS CoV-2. The initial lung X-ray revealed prominent bronchovascular marking in the pulmonary parenchyma, with bilaterally reduced transparency, basally. The position and size of the hiluses was normal. The costophrenic angles were sharp and transparent. Both hemidiaphragms were sharp and well defined (Figure 1).

06f01

Figure 1. Prominent bronchovascular marking, with bilaterally reduced basal transparency

06f02

Figure 2. Pleural effusion with fibroadhesive lesions basally, on the right

06f03

Figure 3. Slightly reduced transparency of the pulmonary parenchyma on the right, first positionally. There is no consolidation in the pulmonary parenchyma. Diffusely accentuated interstitial pattern. Hilar shadows of normal width, vascular. Radiographically without definitive signs of pleural effusion. Pleural adhesions, bilaterally basally, more pronounced on the right

During hospitalization, the patient was treated according to the protocol for treating COVID-19 patients. Gradually, her status improved, her symptoms subsided, and she was taken off oxygen therapy. On the 10th day of hospitalization, pleural effusion developed (Figure 2), which subsided very quickly and was not visible on repeat X-ray, after four days (Figure 3). On the 16th day of hospitalization, the patient was discharged with a good general health status.

DISCUSSION

We present a case of pleural effusion in a COVID-19 female patient, in whom pleural effusion developed at a later stage of the progression of disease (Figure 2), which coincides with what Salehi et al. reported in their study [6], while Zhang et al. reported on a case of COVID-19 with pleural effusion as an initial symptom [12]. Song et al. found that pleural effusion resolved after two days [10]. In our patient, as well, a repeat X-ray, four days later, showed that the pleural effusion had disappeared (Figure 3). Some studies show that the frequency of pleural effusions varies depending on age [11],[13]. In their study involving 552 patients, Majidi et al. showed that pleural effusion developed more often in patients aged 50 years and older [13]. In their study, Wei et al. also demonstrated that patients who had developed pleural effusion during COVID-19 were significantly older (60.8 ± 15.4 years) and that they had an underlying respiratory disease registered in their medical history [11]. Our patient was 49 years old, without comorbidities, which may indicate that if a patient is younger than 60 years and without comorbidities, this does not necessarily mean that they are completely without risk of pleural effusion.

Studies have shown that laboratory findings demonstrate differences between patients with pleural effusion and those without pleural effusion. Patients with pleural effusion had a higher white blood cell count, neutrophil count, platelet count, as well as higher values of CRP and the erythrocyte sedimentation rate, as compared to patients without pleural effusion. This indicates severe inflammation in patients with pleural effusion [11], which was not the case with our patient. Our patient had a white blood cell count and neutrophil count within the reference ranges, throughout her hospital treatment. Normally, increased levels of CRP and an elevated platelet count are indicators of poor prognosis in COVID-19 patients [14]. Wei et al. report a greater number of patients with pleural effusion whose CRP levels were elevated as compared to the number of patients without pleural effusion but with elevated CRP levels [11]. Our patient also had CRP values above the reference range, while the thrombocyte count at admission was within the reference range, while further, during hospitalization, this value was above the reference range. A large study including 476 COVID-19 patients, carried out by Feng et al., also showed that the incidence of pleural effusion was significantly higher in patients with severe clinical presentation, as compared to patients who presented with a milder form [15]. Similar findings were recorded in some other studies, which showed that the frequency of pleural effusion was significantly higher in patients with severe clinical presentation of COVID-19 than in patients with milder presentation [7],[8],[16],[17],[18]. However, this was not the case with our patient, who did not have a severe clinical presentation and was discharged on the 16th day of hospitalization, cured of disease.

CONCLUSION

Although this case has its limitations, regarding the lack of additional radiological and laboratory diagnostics, it nevertheless offers insight into the course and prognosis of disease that is different from what has been reported so far in the studies related to this field. Our experience has shown that pleural effusion may develop even in younger patients who have no comorbidities and whose clinical presentation of COVID-19 is not severe.

LIST OF ABBREVIATIONS AND ACRONYMS

RBC – Red blood cell count (erythrocyte count)
WBC – White blood cell count (leukocyte count)
ANC – Absolute neutrophil count
Lymphs – Lymphocytes
Mo – Monocytes
PLT – Platelets (thrombocytes)
CRP – C-reactive protein
TP – Total protein
Alb – Albumin
ALT – Alanine aminotransferase
AST – Aspartate aminotransferase
ALP – Alkaline phosphatase
LDH – Lactate dehydrogenase
CK – Creatinine kinase

  • Conflict of interest:
    None declared.

Informations

Volume 2 No 4

December 2021

Pages 371-376
  • Keywords:
    COVID-19, pleural effusions, chest radiography
  • Received:
    30 October 2021
  • Revised:
    16 November 2021
  • Accepted:
    28 November 2021
  • Online first:
    13 December 2021
  • DOI:
  • Cite this article:
    Aritonović-Pribaković J, Perić M, Milošević J, Janićević A. Pleural effusion in a COVID-19 patient. Serbian Journal of the Medical Chamber. 2021;2(4):371-6. doi: 10.5937/smclk2-34669
Corresponding author

Jelena Aritonović Pribaković
University of Pristina-Kosovska Mitrovica,
Faculty of Medicine Kosovska Mitrovica, Serbia
10/3 Kalovita Street, 11000, 11100 Belgrade, Serbia
E-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.


  • 1. Zhou S, Wang Y, Zhu T, Xia L. CT Features of Coronavirus Disease 2019 (COVID-19) Pneumonia in 62 Patients in Wuhan, China. AJR Am J Roentgenol. 2020 Jun;214(6):1287-1294. doi: 10.2214/AJR.20.22975.[CROSSREF]

    2. 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 Apr;295(1):202-207. doi: 10.1148/radiol.2020200230.[CROSSREF]

    3. ACR recommendations for the use of chest radiography and computed tomography

    4. (CT) for suspected COVID-19 infection. American College of Radiology. Dostupno na: https://www.acr.org/Advocacy-and-Economics/ACR-Position-Statements/Recommendations-for-Chest-Radiography-and-CT-for-Suspected-COVID19-Infection. [HTTP]

    5. Jacobi A, Chung M, Bernheim A, Eber C. Portable chest X-ray in coronavirus disease-19 (COVID-19): A pictorial review. Clin Imaging. 2020 Aug;64:35-42. doi: 10.1016/j.clinimag.2020.04.001. [CROSSREF]

    6. Ng MY, Lee EYP, Yang J, Yang F, Li X, Wang H, et al. Imaging Profile of the COVID-19 Infection: Radiologic Findings and Literature Review. Radiol Cardiothorac Imaging. 2020 Feb 13;2(1):e200034. doi: 10.1148/ryct.2020200034.[CROSSREF]

    7. Salehi S, Abedi A, Balakrishnan S, Gholamrezanezhad A. Coronavirus Disease 2019 (COVID-19): A Systematic Review of Imaging Findings in 919 Patients. AJR Am J Roentgenol. 2020 Jul;215(1):87-93. doi: 10.2214/AJR.20.23034.[CROSSREF]

    8. Chong WH, Saha BK, Conuel E, Chopra A. The incidence of pleural effusion in COVID-19 pneumonia: State-of-the-art review. Heart Lung. 2021 JulAug;50(4):481-90. doi: 10.1016/j.hrtlng.2021.02.015.[CROSSREF]

    9. Saha BK, Chong WH, Austin A, Kathuria R, Datar P, Shkolnik B, et al. Pleural abnormalities in COVID-19: a narrative review. J Thorac Dis. 2021 Jul;13(7):4484-99. doi: 10.21037/jtd-21-542.[CROSSREF]

    10. Chong WH, Huggins JT, Chopra A. Characteristics of Pleural Effusion in Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Pneumonia. Am J Med Sci. 2021 Feb;361(2):281-4. doi: 10.1016/j.amjms.2020.09.008.[CROSSREF]

    11. Song F, Shi N, Shan F, Zhang Z, Shen J, Lu H, et al. Emerging 2019 Novel Coronavirus (2019-nCoV) Pneumonia. Radiology. 2020 Apr;295(1):210-7. doi: 10.1148/radiol.2020200274.[CROSSREF]

    12. Wei XS, Wang X, Ye LL, Niu YR, Peng WB, Wang ZH, et al. Pleural effusion as an indicator for the poor prognosis of COVID-19 patients. Int J Clin Pract. 2021 Jun;75(6):e14123. doi: 10.1111/ijcp.14123.[CROSSREF]

    13. Zhang J, Chai C, Li L, Qu M, Duan H, Ren L, et al. COVID-19 with pleural effusion as the initial symptom: a case study analysis. Ann Palliat Med. 2020 Sep;9(5):3710-5. doi: 10.21037/apm-20-1720.[CROSSREF]

    14. Majidi H, Bani-Mostafavi ES, Mardanshahi Z, Godazandeh F, Ghasemian R, Heydari K, et al. High-resolution computed tomography finding in 552 patients with symptomatic COVID-19: first report from north of Iran. Emerg Radiol. 2020 Dec;27(6):633-9. doi: 10.1007/s10140-020-01819-9.[CROSSREF]

    15. Bao J, Li C, Zhang K, Kang H, Chen W, Gu B. Comparative analysis of laboratory indexes of severe and non-severe patients infected with COVID-19. Clin Chim Acta. 2020 Oct;509:180-94. doi: 10.1016/j.cca.2020.06.009.[CROSSREF]

    16. Feng Y, Ling Y, Bai T, Xie Y, Huang J, Li J, et al. COVID-19 with Different Severities: A Multicenter Study of Clinical Features. Am J Respir Crit Care Med. 2020 Jun 1;201(11):1380-8. doi: 10.1164/rccm.202002-0445OC.[CROSSREF]

    17. Fu Z, Tang N, Chen Y, Ma L, Wei Y, Lu Y, et al. CT features of COVID-19 patients with two consecutive negative RT-PCR tests after treatment. Sci Rep. 2020 Jul 14;10(1):11548. doi: 10.1038/s41598-020-68509-x.[CROSSREF]

    18. Li K, Fang Y, Li W, Pan C, Qin P, Zhong Y, et al. CT image visual quantitative evaluation and clinical classification of coronavirus disease (COVID-19). Eur Radiol. 2020 Aug;30(8):4407-16. doi: 10.1007/s00330-020-06817-6.[CROSSREF]

    19. Tabatabaei SMH, Talari H, Moghaddas F, Rajebi H. CT Features and Shortterm Prognosis of COVID-19 Pneumonia: A Single-Center Study from Kashan, Iran. Radiol Cardiothorac Imaging. 2020 Apr 20;2(2):e200130. doi: 10.1148/ ryct.2020200130. [CROSSREF]


REFERENCES

1. Zhou S, Wang Y, Zhu T, Xia L. CT Features of Coronavirus Disease 2019 (COVID-19) Pneumonia in 62 Patients in Wuhan, China. AJR Am J Roentgenol. 2020 Jun;214(6):1287-1294. doi: 10.2214/AJR.20.22975.[CROSSREF]

2. 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 Apr;295(1):202-207. doi: 10.1148/radiol.2020200230.[CROSSREF]

3. ACR recommendations for the use of chest radiography and computed tomography

4. (CT) for suspected COVID-19 infection. American College of Radiology. Dostupno na: https://www.acr.org/Advocacy-and-Economics/ACR-Position-Statements/Recommendations-for-Chest-Radiography-and-CT-for-Suspected-COVID19-Infection. [HTTP]

5. Jacobi A, Chung M, Bernheim A, Eber C. Portable chest X-ray in coronavirus disease-19 (COVID-19): A pictorial review. Clin Imaging. 2020 Aug;64:35-42. doi: 10.1016/j.clinimag.2020.04.001. [CROSSREF]

6. Ng MY, Lee EYP, Yang J, Yang F, Li X, Wang H, et al. Imaging Profile of the COVID-19 Infection: Radiologic Findings and Literature Review. Radiol Cardiothorac Imaging. 2020 Feb 13;2(1):e200034. doi: 10.1148/ryct.2020200034.[CROSSREF]

7. Salehi S, Abedi A, Balakrishnan S, Gholamrezanezhad A. Coronavirus Disease 2019 (COVID-19): A Systematic Review of Imaging Findings in 919 Patients. AJR Am J Roentgenol. 2020 Jul;215(1):87-93. doi: 10.2214/AJR.20.23034.[CROSSREF]

8. Chong WH, Saha BK, Conuel E, Chopra A. The incidence of pleural effusion in COVID-19 pneumonia: State-of-the-art review. Heart Lung. 2021 JulAug;50(4):481-90. doi: 10.1016/j.hrtlng.2021.02.015.[CROSSREF]

9. Saha BK, Chong WH, Austin A, Kathuria R, Datar P, Shkolnik B, et al. Pleural abnormalities in COVID-19: a narrative review. J Thorac Dis. 2021 Jul;13(7):4484-99. doi: 10.21037/jtd-21-542.[CROSSREF]

10. Chong WH, Huggins JT, Chopra A. Characteristics of Pleural Effusion in Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Pneumonia. Am J Med Sci. 2021 Feb;361(2):281-4. doi: 10.1016/j.amjms.2020.09.008.[CROSSREF]

11. Song F, Shi N, Shan F, Zhang Z, Shen J, Lu H, et al. Emerging 2019 Novel Coronavirus (2019-nCoV) Pneumonia. Radiology. 2020 Apr;295(1):210-7. doi: 10.1148/radiol.2020200274.[CROSSREF]

12. Wei XS, Wang X, Ye LL, Niu YR, Peng WB, Wang ZH, et al. Pleural effusion as an indicator for the poor prognosis of COVID-19 patients. Int J Clin Pract. 2021 Jun;75(6):e14123. doi: 10.1111/ijcp.14123.[CROSSREF]

13. Zhang J, Chai C, Li L, Qu M, Duan H, Ren L, et al. COVID-19 with pleural effusion as the initial symptom: a case study analysis. Ann Palliat Med. 2020 Sep;9(5):3710-5. doi: 10.21037/apm-20-1720.[CROSSREF]

14. Majidi H, Bani-Mostafavi ES, Mardanshahi Z, Godazandeh F, Ghasemian R, Heydari K, et al. High-resolution computed tomography finding in 552 patients with symptomatic COVID-19: first report from north of Iran. Emerg Radiol. 2020 Dec;27(6):633-9. doi: 10.1007/s10140-020-01819-9.[CROSSREF]

15. Bao J, Li C, Zhang K, Kang H, Chen W, Gu B. Comparative analysis of laboratory indexes of severe and non-severe patients infected with COVID-19. Clin Chim Acta. 2020 Oct;509:180-94. doi: 10.1016/j.cca.2020.06.009.[CROSSREF]

16. Feng Y, Ling Y, Bai T, Xie Y, Huang J, Li J, et al. COVID-19 with Different Severities: A Multicenter Study of Clinical Features. Am J Respir Crit Care Med. 2020 Jun 1;201(11):1380-8. doi: 10.1164/rccm.202002-0445OC.[CROSSREF]

17. Fu Z, Tang N, Chen Y, Ma L, Wei Y, Lu Y, et al. CT features of COVID-19 patients with two consecutive negative RT-PCR tests after treatment. Sci Rep. 2020 Jul 14;10(1):11548. doi: 10.1038/s41598-020-68509-x.[CROSSREF]

18. Li K, Fang Y, Li W, Pan C, Qin P, Zhong Y, et al. CT image visual quantitative evaluation and clinical classification of coronavirus disease (COVID-19). Eur Radiol. 2020 Aug;30(8):4407-16. doi: 10.1007/s00330-020-06817-6.[CROSSREF]

19. Tabatabaei SMH, Talari H, Moghaddas F, Rajebi H. CT Features and Shortterm Prognosis of COVID-19 Pneumonia: A Single-Center Study from Kashan, Iran. Radiol Cardiothorac Imaging. 2020 Apr 20;2(2):e200130. doi: 10.1148/ ryct.2020200130. [CROSSREF]

1. Zhou S, Wang Y, Zhu T, Xia L. CT Features of Coronavirus Disease 2019 (COVID-19) Pneumonia in 62 Patients in Wuhan, China. AJR Am J Roentgenol. 2020 Jun;214(6):1287-1294. doi: 10.2214/AJR.20.22975.[CROSSREF]

2. 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 Apr;295(1):202-207. doi: 10.1148/radiol.2020200230.[CROSSREF]

3. ACR recommendations for the use of chest radiography and computed tomography

5. Jacobi A, Chung M, Bernheim A, Eber C. Portable chest X-ray in coronavirus disease-19 (COVID-19): A pictorial review. Clin Imaging. 2020 Aug;64:35-42. doi: 10.1016/j.clinimag.2020.04.001. [CROSSREF]

6. Ng MY, Lee EYP, Yang J, Yang F, Li X, Wang H, et al. Imaging Profile of the COVID-19 Infection: Radiologic Findings and Literature Review. Radiol Cardiothorac Imaging. 2020 Feb 13;2(1):e200034. doi: 10.1148/ryct.2020200034.[CROSSREF]

7. Salehi S, Abedi A, Balakrishnan S, Gholamrezanezhad A. Coronavirus Disease 2019 (COVID-19): A Systematic Review of Imaging Findings in 919 Patients. AJR Am J Roentgenol. 2020 Jul;215(1):87-93. doi: 10.2214/AJR.20.23034.[CROSSREF]

8. Chong WH, Saha BK, Conuel E, Chopra A. The incidence of pleural effusion in COVID-19 pneumonia: State-of-the-art review. Heart Lung. 2021 JulAug;50(4):481-90. doi: 10.1016/j.hrtlng.2021.02.015.[CROSSREF]

9. Saha BK, Chong WH, Austin A, Kathuria R, Datar P, Shkolnik B, et al. Pleural abnormalities in COVID-19: a narrative review. J Thorac Dis. 2021 Jul;13(7):4484-99. doi: 10.21037/jtd-21-542.[CROSSREF]

10. Chong WH, Huggins JT, Chopra A. Characteristics of Pleural Effusion in Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Pneumonia. Am J Med Sci. 2021 Feb;361(2):281-4. doi: 10.1016/j.amjms.2020.09.008.[CROSSREF]

11. Song F, Shi N, Shan F, Zhang Z, Shen J, Lu H, et al. Emerging 2019 Novel Coronavirus (2019-nCoV) Pneumonia. Radiology. 2020 Apr;295(1):210-7. doi: 10.1148/radiol.2020200274.[CROSSREF]

12. Wei XS, Wang X, Ye LL, Niu YR, Peng WB, Wang ZH, et al. Pleural effusion as an indicator for the poor prognosis of COVID-19 patients. Int J Clin Pract. 2021 Jun;75(6):e14123. doi: 10.1111/ijcp.14123.[CROSSREF]

13. Zhang J, Chai C, Li L, Qu M, Duan H, Ren L, et al. COVID-19 with pleural effusion as the initial symptom: a case study analysis. Ann Palliat Med. 2020 Sep;9(5):3710-5. doi: 10.21037/apm-20-1720.[CROSSREF]

14. Majidi H, Bani-Mostafavi ES, Mardanshahi Z, Godazandeh F, Ghasemian R, Heydari K, et al. High-resolution computed tomography finding in 552 patients with symptomatic COVID-19: first report from north of Iran. Emerg Radiol. 2020 Dec;27(6):633-9. doi: 10.1007/s10140-020-01819-9.[CROSSREF]

15. Bao J, Li C, Zhang K, Kang H, Chen W, Gu B. Comparative analysis of laboratory indexes of severe and non-severe patients infected with COVID-19. Clin Chim Acta. 2020 Oct;509:180-94. doi: 10.1016/j.cca.2020.06.009.[CROSSREF]

16. Feng Y, Ling Y, Bai T, Xie Y, Huang J, Li J, et al. COVID-19 with Different Severities: A Multicenter Study of Clinical Features. Am J Respir Crit Care Med. 2020 Jun 1;201(11):1380-8. doi: 10.1164/rccm.202002-0445OC.[CROSSREF]

17. Fu Z, Tang N, Chen Y, Ma L, Wei Y, Lu Y, et al. CT features of COVID-19 patients with two consecutive negative RT-PCR tests after treatment. Sci Rep. 2020 Jul 14;10(1):11548. doi: 10.1038/s41598-020-68509-x.[CROSSREF]

18. Li K, Fang Y, Li W, Pan C, Qin P, Zhong Y, et al. CT image visual quantitative evaluation and clinical classification of coronavirus disease (COVID-19). Eur Radiol. 2020 Aug;30(8):4407-16. doi: 10.1007/s00330-020-06817-6.[CROSSREF]

19. Tabatabaei SMH, Talari H, Moghaddas F, Rajebi H. CT Features and Shortterm Prognosis of COVID-19 Pneumonia: A Single-Center Study from Kashan, Iran. Radiol Cardiothorac Imaging. 2020 Apr 20;2(2):e200130. doi: 10.1148/ ryct.2020200130. [CROSSREF]


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