Pleurisy and pericarditis as a cause of atypical chest pain in patients with in early post-COVID-19 period

During the pandemic COVID-19, there has been an increase in the number of patients with non-anginal chest pain at cardiologist appointments.

Objective. To assess the incidence of signs of pleurisy and pericarditis after COVID-19 in non-comorbid patients with atypical chest pain and describe their characteristics according to echocardiography and magnetic resonance imaging.

Materials and methods. From February 2021 to January 2022, 200 outpatients were prospectively enrolled in the study, all of them suffered from a discomfort in the heart region for the first time after SARS-CoV-2 infection. Inclusion criteria: 18–50 years old, 5–12 weeks after SARS-CoV-2 infection, non-anginal chest pain. Exclusion criteria: pneumonia or signs of pulmonary thromboembolism, coronary heart disease, congestive heart failure or kidney disease, clinical or laboratory signs of myocarditis, oncopathology, radiation or chemotherapy of the chest in past medical history. A survey was conducted (yes/no) for the presence of general malaise, quality of life deterioration, hyperthermia, cough. Ultrasound examination of the pericardium and pleura to detect effusion or postinflammatory changes was performed in accordance with the recommendations. Magnetic resonance imaging was performed if ultrasound imaging was poor or there was no evidence of pericardial or pleural involvement in patients with typical symptoms.

Results. 82 women and 118 men were included. Median of age 39 [28–46] years old. Pericarditis was diagnosed in 152 (76%) patients, including effusive pericarditis in 119 (78%), myocarditis in 6 (3%) and myopericarditis

in 49 (25%) patients, pleurisy was detected in 22 (11%) patients, exudative pleurisy – in 11 (5.5%) patients with a predominant unilateral lesion of the mediastinal-diaphragmatic region adjacent to the heart. Hyperthermia was recorded in 2.5% of cases, general malaise – in 60% and a decrease in the quality of life – in 84%.

Conclusion. Serositis as a cause of atypical chest pain among young non-comorbid patients in early postCOVID was identified in 87% of patients. In the coming years, it is probably worthwhile to perform ultrasound of the pericardium and pleura in all patients with chest pain.

1. Nasonov E.L. Coronavirus disease 2019 (COVID-19): a rheumatologist’s thoughts. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2020; 58 (2): 123–132 http://doi.org/10.14412/1995-4484-2020-123-132 (In Russian)

2. Wang D., Hu B., Hu C., Zhu F. et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus–infected pneumonia in Wuhan, China. JAMA. 2020; 323 (11): 1061–1069. http://doi.org/10.1001/jama.2020.1585.

3. Sukmarova Z.N., Simonenko V.B., Ibragimova F.M., Demyanenko A.V. Pericardial eff usion as a new specific symptom of SARS-CoV-2. Clinical Medicine (Russian Journal). 2021; 99 (3):192–197. http://doi.org/10.30629/0023-2149-2021-99-3-192-197 (In Russian)

4. Sukmarova Z., Saidova M.A. Echocardiographic phenomenon of pericarditis in patients with severe COVID-19 pneumonia. One-year observation. Eur. Heart J. – Cardiovasc. Imaging. 2022; 23 (1): jeab289.278. http://doi.org/10.1093/ehjci/jeab289.278

5. Diaz-Arocutipa C., Saucedo-Chinchay J., Imazio M. Pericarditis in patients with COVID-19: a systematic review. J. Cardiovasc. Med. (Hagerstown). 2021; 22 (9): 693–700. http://doi.org/10.2459/JCM.0000000000001202

6. Cosyns B., Plein S., Nihoyanopoulos P. et al.; on behalf of the European Association of Cardiovascular Imaging (EACVI) and European Society of Cardiology Working Group (ESC WG) on Myocardial and Pericardial diseases. European Association of Cardiovascular Imaging (EACVI) position paper: multimodality imaging in pericardial disease. Eur. Heart J. Cardiovasc. Imaging. 2014; 16: 12–31.

7. Hallifax R.J., Talwar A., Wrightson J.M. et al. State-ofthe-art: Radiological investigation of pleural disease. Respir. Med. 2017; 124: 88–99. http://doi.org/10.1016/j.rmed.2017.02.013

8. Jany B., Welte T. Pleural Effusion in Adults-Etiology, Diagnosis, and Treatment. Dtsch. Arztebl. Int. 2019; 116 (21): 377–386. http://doi.org/10.3238/arztebl.2019.0377

9. Sinitsyn V.E., Stukalova O.V., Larina O.M., Ternovoy S.K. New possibilities for diagnosing non-coronary myocardial lesions: the role of magnetic resonance imaging. Creative cardiology. 2008; 1: 66–73. (In Russian)

10. Akhadov T.A., Guryakov S.Yu., Ublinsky M.V. Magnetic resonance imaging in study of lungs. Medical Visualization. 2019; 23 (4): 10–23. http://doi.org/10.24835/1607-0763-2019-4-10-23 (In Russian)

11. Imazio M., Demichelis B., Parrini I. et al. Recurrent pain without objective evidence of disease in patients with previous idiopathic or viral acute pericarditis. Am. J. Cardiol. 2004; 94: 973–975. http://doi.org/10.1016/j.amjcard.2004.06.046

12. Boniface N., Kley J., Lisko J. et al. Non-cardiac chest pain: Is it really? Circulation. 2014; 130: A12863.

13. Morgenstern D., Kley J., Lisko J. et al. Chest pain in patients under age 40: Are we getting it right? J. Am. Coll. Cardiol. 2015; 65 (10S).

14. Ramadan M.S., Bertolino L., Zampino R., DuranteMangoni E.; Monaldi Hospital Cardiovascular Infection Study Group. Cardiac sequelae after coronavirus disease 2019 recovery: a systematic review. Clin. Microbiol. Infect. 2021; 27 (9): 1250–1261. http://doi.org/10.1016/j.cmi.2021.06.015

15. Puntmann V.O., Carerj M.L., Wieters I. et al. Outcomes of Cardiovascular Magnetic Resonance Imaging in Patients Recently Recovered From Coronavirus Disease 2019 (COVID-19). JAMA Cardiol. 2020; 5 (11): 1265–1273. http://doi.org/10.1001/jamacardio.2020.3557

16. Chong W.H., Saha B.K., Conuel E., Chopra A. The incidence of pleural effusion in COVID-19 pneumonia: State-of-the-art review. Heart Lung. 2021; 50 (4): 481– 490. http://doi.org/10.1016/j.hrtlng.2021.02.015

17. Walker S.P., Morley A.J., Stadon L. et al. Nonmalignant Pleural Effusions: A Prospective Study of 356 Consecutive Unselected Patients. Chest. 2017; 151 (5): 1099–1105. http://doi.org/10.1016/j.chest.2016.12.014

18. Menéndez R., Torres A., Zalacaín R. et al.; Neumofail Group. Risk factors of treatment failure in community acquired pneumonia: implications for disease outcome. Thorax. 2004; 59 (11): 960–965. http://doi.org/10.1136/thx.2003.017756

19. Lan C.C., Hsu H.H., Wu C.P. et al. Influences of pleural effusion on respiratory mechanics, gas exchange, hemodynamics, and recruitment effects in acute respiratory distress syndrome. J. Surg. Res. 2014; 186 (1): 346–353. http://doi.org/10.1016/j.jss.2013.09.002

20. Hasley P.B., Albaum M.N., Li Y.H. et al. Do pulmonary radiographic findings at presentation predict mortality in patients with community-acquired pneumonia? Arch. Intern. Med. 1996; 156 (19): 2206–2212

21. Zhao W., Zhong Z., Xie X. et al. Relation between chest CT findings and clinical conditions of coronavirus disease (COVID-19) pneumonia: a multicenter study. Am. J. Roentgenol. 2020; 214 (5): 1072–1077. http://doi.org/10.2214/AJR.20.22976

22. Li K., Fang Y., Li W. CT image visual quantitative evaluation and clinical classification of coronavirus disease (COVID-19) Eur. Radiol. 2020; 30 (8): 4407–4416. http://doi.org/10.1007/s00330-020-06817-6

23. Majidi H., Bani-Mostafavi E.S., Mardanshahi Z. Highresolution computed tomography finding in 552 patients with symptomatic COVID-19: first report from north of Iran. Emerg. Radiol. 2020; 27 (6): 633–639. http://doi.org/10.1007/s10140-020-01819-9

24. Chen A., Huang J., Liao Y. Differences in clinical and imaging presentation of pediatric patients with COVID-19 in comparison with adults. Radiol.: Cardiothorac. Imaging. 2020; 2 (2). http://doi.org/10.1148/ryct.2020200117

25. Fahad A.M., Al-Khalidi H.A., Abdulhameed Alhaideri Y.A. et al. Pleural effusion in a patient with COVID-19 pneumonia and lung cancer: a case report. Respir. Med. Case Rep. 2020; 31. http://doi.org/10.1016/j.rmcr.2020.101302

26. Tham S.M., Lim W.Y., Lee C.K. Four patients with COVID-19 and tuberculosis, Singapore, April–May 2020. Emerg. Infect. Dis. 2020; 26 (11): 2763–2765. http://doi.org/10.3201/eid2611.202752.

27. Le Roux P., Millardet E., Duquenoy A. etal. Pleuropneumonia resulting from varicella and COVID-19 co-infection in a 10-month-old infant. Arch. Pediatr. 2020; 27 (8): 509–510. http://doi.org/10.1016/j.arcped.2020.08.001

28. Yamaguchi Y., Hashimoto M., Saito S. et al. Suspected Tuberculous Pleurisy and Coronavirus Disease 2019 Comorbidity. Intern. Med. 2022; 61 (6): 913–916. http://doi.org/10.2169/internalmedicine.6920-21

29. Hussein M., Haq I.U., Hameed M. et al. Pleural effusion as an isolated finding in COVID-19 infection. Respir. Med. Case Rep. 2020; 31: 101269. http://doi.org/10.1016/j.rmcr.2020.101269

30. Oleynick C. Symptoms of Pleurisy as the Initial Presentation of COVID-19. Am. J. Case Rep. 2020; 21: e925775. http://doi.org/10.12659/AJCR.925775.

31. Bao C., Liu X., Zhang H. et al. Coronavirus Disease 2019 (COVID-19) CT Findings: A Systematic Review and Metaanalysis. J. Am. Coll. Radiol. 2020; 17 (6): 701–709. http://doi.org/10.1016/j.jacr.2020.03.006

32. Li Y., Cao J., Zhang X. et al. Chest CT imaging characteristics of COVID-19 pneumonia in preschool children: a retrospective study. BMC Pediatr. 2020; 20 (1): 227. http://doi.org/10.1186/s12887-020-02140-7

33. Bai H.X., Hsieh B., Xiong Z. et al. Performance of Radiologists in Differentiating COVID-19 from Non-COVID-19 Viral Pneumonia at Chest CT. Radiology. 2020; 296 (2): E46–E54. http://doi.org/10.1148/radiol.2020200823

34. Vasilev Y.A., Sergunova K.A., Bazhin A.V. et al. Chest MRI of patients with COVID-19. Magn. Reson. Imaging. 2021; 79: 13–19. http://doi.org/10.1016/j.mri.2021.03.005

35. Most Z.M., Hendren N., Drazner M.H., Perl T.M. Striking Similarities of Multisystem Inflammatory Syndrome in Children and a Myocarditis-Like Syndrome in Adults Overlapping Manifestations of COVID-19. Circulation. 2021; 143: 4. http://doi.org/610.1161/CIRCULATIONAHA.120.050166

36. Winant A.J., Blumfield E., Liszewski M.C. et al. Thoracic imaging findings of multisystem inflammatory syndrome in children (MIS-C) associated with COVID-19: what radiologists need to know now. Radiology: Cardiothorac. Imaging. 2020; 2 (4). http://doi.org/10.1148/ryct.2020200346

37. Насонов Е.Л. Российские клинические рекомендации. Ревматология. М.: ГЭОТАР-Медиа, 2017. 464 с. ISBN 978-5-9704-4261-6. Nasonov E.L. Russian clinical guidelines. Rheumatology. Moscow: GEOTAR-Media, 2017. 464 p. ISBN 978-5-9704-4261-6 (In Russian)

38. Blumfield E., Levin T.L., Kurian J. et al. Imaging findings in multisystem inflammatory syndrome in children (MIS-C) associated with coronavirus disease (COVID-19) Am. J. Roentgenol. 2021; 216 (2): 507–517. http://doi.org/10.2214/AJR.20.24032

39. Winant A.J., Blumfield E., Liszewski M.C. et al. Thoracic imaging findings of multisystem inflammatory syndrome in children (MIS-C) associated with COVID-19: what radiologists need to know now. Radiology: Cardiothorac. Imaging. 2020; 2 (4). http://doi.org/10.1148/ryct.2020200346

40. Hameed S., Elbaaly H., Reid C.E.L. Spectrum of imaging findings at chest radiography, US, CT, and MRI in multisystem inflammatory syndrome in children associated with COVID-19. Radiology. 2021; 298 (1): E1–E10. http://doi.org/10.1148/radiol.2020202543

41. Rodríguez Y., Novelli L., Rojas M. et al. Autoinflammatory and autoimmune conditions at the crossroad of COVID-19. J. Autoimmun. 2020; 114: 102506. http://doi.org/10.1016/j.jaut.2020.102506

42. Harris E., Shanghavi S., Viner T. Polyserositis secondary to COVID-19: the diagnostic dilemma. BMJ Case Rep. 2021; 14 (9): e243880. http://doi.org/10.1136/bcr-2021-243880

43. Losada I., González-Moreno J., Roda N. et al. Polyserositis: a diagnostic challenge. Intern. Med. J. 2018; 48 (8): 982–987. http://doi.org/10.1111/imj.13966

44. Chung M., Bernheim A., Mei X. et al. CT imaging features of 2019 novel coronavirus (2019-nCoV). Radiology. 2020; 295 (1): 202–207. http://doi.org/10.1148/radiol.2020200230

45. Ussov W.Yu., Nudnov N.V., Ignatenko G.A., Gulyaev V.M., Pervak M.B., Shelkovnikova T.A., Dubovaya A.V., Bergen T.A. Primary and prospective imaging of the chest using magnetic resonance imaging in patients with viral lung damage in COVID-19. Medical Visualization. 2020; 24 (4): 11–26. http://doi.org/10.24835/1607-0763-2020-4-11-26 (In Russian)