Generate QR code
Open Access
Subscription Access
Pericardial effusion in coronavirus infection
https://doi.org/10.30629/0023-2149-2025-103-4-249-262
Abstract
The issue of pericardial effusion concerns a wide range of nosologies. Today, it is particularly relevant in connection with post-COVID complications and new cases of this cardiotropic infection. Managing hydropneumopericardium raises numerous questions: from diagnostic criteria and assessing “significance” to the necessity of therapy and the choice of methods. This lecture compiles all key points regarding the management of effusion in the pericardial cavity, systematizes the approach to diagnosis and treatment, details the most challenging dilemmas that arise when managing such patients, and offers examples and personal insights into decision-making based on the experience of treating nearly a thousand patients.
About the Authors
Z. N. Sukmarova
V.A. Nasonova Research Institute of Rheumatology
Russian Federation
Russian Federation
Zulfiya N. Sukmarova — Candidate of Medical Sciences, Researcher,
Cardiologist
Moscow
M. A. Saidova
E.I. Chazov National Medical Research Center of Cardiology
Russian Federation
Russian Federation
Marina A. Saidova — Doctor of Medical Sciences, Professor, Head of the Department of Functional Diagnostics
Moscow
M. K. Rybakova
Russian Medical Academy of Continuous Postgraduate Education of the Ministry of Health
Russian Federation
Russian Federation
Marina K. Rybakova — Doctor of Medical Sciences, Professor of Ultrasound Diagnostics
Moscow
References
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. (In Russian)]. DOI: 10.14412/1995-4484-2020-123-132
2. Li P., Shi A., Lu X., Li C., Cai P., Teng C. et al. Incidence and impact of acute pericarditis in hospitalized COVID-19 patients. J. Am. Heart Assoc. 2023;12:e028970. DOI: 10.1161/JAHA.122.028970
3. Buckley B.J.R., Harrison S.L., Fazio-Eynullayeva E., Underhill P., Lane D.A., Lip G.Y.H. Prevalence and clinical outcomes of myocarditis and pericarditis in 718,365 COVID-19 patients. Eur. J. Clin. Invest. 2021;51(11):e13679. DOI: 10.1111/eci.13679
4. Adler Y., Charron P., Imazio M., Badano L., Barón-Esquivias G., Bogaert J. et al. ESC Scientifi c Document Group. 2015 ESC Guidelines for the diagnosis and management of pericardial diseases: The task force for the diagnosis and management of pericardial diseases of the european society of cardiology (ESC) Endorsed by: the european association for cardio-thoracic surgery (EACTS). Eur. Heart J. 2015;36(42):2921–2964. DOI: 10.1093/eurheartj/ehv318
5. Iskandar R., Liu S., Xiang F., Chen W., Li L., Qin W., Huang F., Chen X. Expression of pericardial fl uid T-cells and related infl ammatory cytokines in patients with chronic heart failure. Exp. Ther. Med. 2017;13(5):1850–1858. DOI: 10.3892/etm.2017.4202
6. Vogiatzidis K., Zarogiannis S.G., Aidonidis I., Solenov E.I., Molyvdas P.A., Gourgoulianis K.I., Hatzoglou C. Physiology of pericardial fl uid production and drainage. Front Physiol. 2015 Mar 18;6:62. DOI: 10.3389/fphys.2015.00062
7. Natanzon A., Kronzon I. Pericardial and pleural eff usions in congestive heart failure-anatomical, pathophysiologic, and clinical considerations. Am. J Med. Sci. 2009;338(3):211–6. DOI: 10.1097/MAJ.0b013e3181a3936f
8. Sukmarova Z.N., Ibragimova F.M., Larina O.M., Gromov A.I., Nasonov E.L. Pleurisy and pericarditis as a cause of atypical chest pain in patients with in early post-COVID-19 period. Medical Visualization. 2022;26(4): 11–22. (In Russian)]. DOI: 10.24835/1607-0763-1232
9. Lazaros G., Imazio M., Tsioufi s P., Lazarou E., Vlachopoulos C., Tsioufi s C. Chronic Pericardial Eff usion: Causes and Management. Can. J. Cardiol. 2023;39(8):1121–1131. DOI: 10.1016/j.cjca.2023.02.003
10. Mitiku TY., Heidenreich PA. A small pericardial eff usion is a marker of increased mortality. Am. Heart J. 2011 Jan;161(1):152–7. DOI: 10.1016/j.ahj.2010.10.007
11. Nasonov E.L., Sukmarova Z.N., Popkova T.V., Belov B.S. Problems of immunopathology and prospects for pharmacotherapy of idiopathic recurrent pericarditis: Using an interleukin 1 inhibitor (anakinra). Nauchno-Prakticheskaya Revmatologia = Rheumatology Science and Practice. 2023;61(1):47-61 (In Russian)]. DOI: 10.47360/1995-4484-2023-47-61
12. https://www.vedomosti.ru/society/articles/2023/06/07/979002-rospotrebnadzor-otmetil-tendentsiyu-k-rostu-zabolevaemosti-tuberkulezom
13. Sinha A., Yeruva SL., Kumar R., Curry B.H. Early Cardiac Tamponade in a Patient with Postsurgical Hypothyroidism. Case Rep. Cardiol. 2015;2015:310350. DOI: 10.1155/2015/310350.
14. Bentata Y., Hamdi F., Chemlal A., Haddiya I., Ismaili N., El Ouafi N. Uremic pericarditis in patients with End Stage Renal Disease: Prevalence, symptoms and outcome in 2017. Am. J. Emerg. Med. 2018 Mar;36(3):464–466. DOI: 10.1016/j.ajem.2017.11.048.
15. Ghantous E., Szekely Y., Lichter Y., Levi E., Taieb P., Banai A. et al. Pericardial involvement in patients hospitalized with COVID-19: prevalence, associates, and clinical implications. J. Am. Heart Assoc. 2022;11(7):e024363. DOI: 10.1161/JAHA.121.024363
16. Ramadan MS., Bertolino L., Zampino R., Durante-Mangoni 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. DOI: 10.1016/j.cmi.2021.06.015
17. Sukmarova Z.N., Potapov E.V., Saidova M.A., Ovchinnikov Yu.V., Gromov A.I. Pericardial involvement associated with SARS-COV-2 infection. Prospective observation in the COVID- ward. REJR. 2022; 12(4):30–47. (In Russian)]. DOI: 10.21569/2222-7415-2022-12-4-30-47
18. Dini F.L., Baldini U., Bytyçi I., Pugliese N.R., Bajraktari G., Henein M.Y. Acute pericarditis as a major clinical manifestation of long COVID-19 syndrome. Int. J. Cardiol. 2023;374:129–134. DOI: 10.1016/j.ijcard.2022.12.019
19. Hanley B., Naresh K.N., Roufosse C., Nicholson A.G., Weir J., Cooke G.S. et al. Histopathological fi ndings and viral tropism in UK patients with severe fatal COVID-19: a post-mortem study. Lancet Microbe. 2020;1(6):e245–e253. DOI: 10.1016/S2666-5247(20)30115-4.
20. Puntmann V.O., Carerj M.L., Wieters I., Fahim M., Arendt C., Hoff mann J. 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. DOI: 10.1001/jamacardio.2020.3557
21. Sukmarova Z.N., Simonenko V.B., Ibragimova F.M., Demyanenko A.V. Pericardial eff usion as a new specifi c symptom of SARS-CoV-2. Klinicheskaya meditsina. 2021;99(3):192–197. (In Russian)]. DOI: 10.30629/0023-2149-2021-99-3-192-197
22. Luk A., Clarke B., Dahdah N., Ducharme A. et al. Myocarditis and pericarditis after Covid-19 mRNA vaccination: practical considerations for care providers. Can. J. Cardiol 2021;37:1629–34.
23. Sukmarova Z.N., Ovchinnikov Yu.V., Gudima G.O. et al. Hyperechogenic signal from the pericardium after vaccination against SARS-CoV-2. Infectious diseases, 2021;19(4):43–50. (In Russian)]. DOI: 10.20953/1729-9225-2021-4-43-50
24. Kermani-Alghoraishi M., Pouramini A., Kafi F., Khosravi A. Coronavirus Disease 2019 (COVID-19) and Severe Pericardial Eff usion: From Pathogenesis to Management: A Case Report Based Systematic Review. Curr. Probl. Cardiol. 2022;47(2):100933. DOI: 10.1016/j.cpcardiol.2021.100933
25. Imazio M., Adler Y. Management of pericardial eff usion. Eur. Heart J. 2013;34(16):1186-97. DOI: 10.1093/eurheartj/ehs372
26. Rybakova M.K., Mitkov V.V. Echocardiography in tables and diagrams. Desktop reference. 3rd ed. VIDAR. 2016. (In Russian). ISBN 978-5-88429-231-4
27. Cosyns B., Plein S., Nihoyanopoulos P., Smiseth O., Achenbach S., Andrade M.J., Pepi M., Ristic A., Imazio M., Paelinck B., Lancel lotti P; European Association of Cardiovascular Imaging (EACVI); European Society of Cardiology Working Group (ESC WG) on Myocardial and Pericardial diseases. European Association of Car diovascular Imaging (EACVI) position paper: Multimodality im aging in pericardial disease. Eur. Heart J. Cardiovasc. Imaging. 2015;16(1):12–31. DOI: 10.1093/ehjci/jeu128
28. Chetrit M., Xu B., Kwon D.H., Ramchand J., Rodriguez R.E., Tan C.D., Jellis C.L., Johnston D.R., Renapurkar RD., Cremer P.C., Klein A.L. Imaging-Guided Therapies for Pericardial Diseases. JACC Cardiovasc Imaging. 2020;13(6):1422–1437. DOI: 10.1016/j.jcmg.2019.08.027
29. Hyeon C.W., Yi H.K., Kim E.K. et al. The role of 18F-fl uorodeoxy glucosee positron emission tomography/computed tomography in the diff erential diagnosis of pericardial disease. Sci. Rep. 2020;10:21524.
30. Burazor I., Aviel-Ronen S., Imazio M., Goitein O., Perelman M., Shelestovich N., Radovanovic N., Kanjuh V., Barshack I., Adler Y. Metastatic cardiac tumors: from clinical presentation through di agnosis to treatment. BMC Cancer. 2018;18(1):202. DOI: 10.1186/s12885-018-4070-x
31. Buoro S., Tombetti E., Ceriotti F., Simon C., Cugola D., Seghez zi M., Innocente F., Maestroni S., Del Carmen Baigorria Vaca M., Moioli V., Previtali G., Manenti B., Adler Y., Imazio M., Bruca to A. What is the normal composition of pericardial fl uid? Heart. 2021;107(19):1584–1590. DOI: 10.1136/heartjnl-2020-317966
32. Humbert M., Kovacs G., Hoeper MM. et al. ESC/ERS Scientifi c Document Group. 2022 ESC/ERS guidelines for the diagnosis and treatment of pulmonary hypertension. Eur. Heart J. 2022;43:3618–731
33. Afonso L, Kottam A, Reddy V, Penumetcha A. Echocardiography in Infective Endocarditis: State of the Art. Curr Cardiol Rep. 2017;19(12):127. doi: 10.1007/s11886-017-0928-9.
34. Sukmarova Z.N., Shishimorov A.A., Parshin V.V., Gromov A.I. Patients monitoring in the City Clinical Hospital No. 52 at the beginning and end of the pandemic. Medical Visualization. (In Russ.). doi:10.24835/1607-0763-1496
35. Søgaard K.K., Farkas D.K., Ehrenstein V., Bhaskaran K., Bøtker H.E., Sørensen H.T. Pericarditis as a marker of occult cancer and a prognostic factor for cancer mortality. Circulation. 2017;136:996–1006
36. Imazio M. Pericardial involvement in systemic infl ammatory diseases. Heart. 2011;97(22):1882–92. DOI: 10.1136/heartjnl-2011-300054
37. Sukmarova Z.N., Saidova M.A., Ovchinnicov Yu.V. Eff usive pericarditis in the pathogenesis of cardiac arrhythmias in COVID-19: a case series. Cardiovascular Therapy and Prevention. 2022;21(2):3021. (In Russian)]. DOI: 10.15829/1728-8800-2022-3021
38. Sukmarova Z.N., Zotkin E.G. Therapy of cardiac arrhythmias associated with SARS-CoV-2 infection with anti-infl ammatory drugs. Clinical medicine. 2023;101(12):665–674. (In Russian). DOI: 10.30629/0023-2149-2023-101-12-665-674
39. Rybakova M.K. Rybakova, Alekhine M.N. Alekhine, Mitkov V.V. Mitkov. A practical guide to ultrasound diagnostics. Echocardiography. VIDAR. Moscow. 2008. (In Russian)].
40. Imazio M., Gaido L., Battaglia A., Gaita F. Contemporary management of pericardial eff usion: practical aspects for clinical practice. Postgrad. Med. 2017;129(2):178–186. DOI: 10.1080/00325481.2017.1285676
41. Ristić A.D., Imazio M., Adler Y., Anastasakis A., Badano L.P., Brucato A., Caforio A.L., Dubourg O., Elliott P., Gimeno J., Helio T., Klingel K., Linhart A., Maisch B., Mayosi B., Mogensen J., Pinto Y., Seggewiss H., Seferović P.M., Tavazzi L., Tomkowski W., Charron P. Triage strategy for urgent management of cardiac tamponade: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur. Heart J. 2014;35(34):2279–84. DOI: 10.1093/eurheartj/ehu217
42. Sagristà-Sauleda J., Angel J., Permanyer-Miralda G, Soler Soler J. Long-term follow-up of idiopathic chronic pericardial eff usion. N. Engl. J. Med. 1999;341(27):2054–9. DOI: 10.1056/NEJM199912303412704
43. Imazio M., Lazaros G., Valenti A., De Carlini C.C., Maggiolini S., Pivetta E., Giustetto C., Tousoulis D., Adler Y., Rinaldi M., Brucato A. Outcomes of idiopathic chronic large pericardial eff usion. Heart. 2019;105(6):477–481. DOI: 10.1136/heartjnl-2018-313532
44. Mitiku T.Y., Heidenreich P.A. A small pericardial eff usion is a marker of increased mortality. Am. Heart J. 2011;161(1):152–7. DOI: 10.1016/j.ahj.2010.10.007
45. Ghosh A.K., Crake T., Manisty C., Westwood M. Pericardial Disease in Cancer Patients. Curr. Treat. Options Cardiovasc. Med. 2018;20(7):60. DOI: 10.1007/s11936-018-0654-7
46. Maisch B., Rupp H., Ristic A., Pankuweit S. Pericardioscopy and epi- and pericardial biopsy — a new window to the heart improving etiological diagnoses and permitting targeted intrapericardial therapy. Heart Fail Rev. 2013;18(3):317–28. DOI: 10.1007/s10741-013-9382-y
47. Fröhlich G.M., Keller P., Schmid F., Wolfrum M., Osranek M., Falk C., Noll G., Enseleit F., Reinthaler M., Meier P., Lüscher T.F., Ruschitzka F., Tanner F.C. Haemodynamically irrelevant pericardial eff usion is associated with increased mortality in patients with chronic heart failure. Eur. Heart J. 2013;34(19):1414–23. DOI: 10.1093/eurheartj/eht006
48. Chen Y.-F., Hsieh M.-R., Chang C.-T., Tsai P.-H., Fang Y.-F. Exploring the Risk Factors for Poor Survival in Lupus Pericarditis Patients: A Retrospective Cohort Study. Journal of Clinical Medicine. 2022;11(18):5473. DOI: 10.3390/jcm11185473
49. De Filippo O., Gatti P., Rettegno S., Iannaccone M., D’Ascenzo F., Lazaros G., Brucato A., Tousoulis D., Adler Y., Imazio M. Is pericardial eff usion a negative prognostic marker? Meta-analysis of outcomes of pericardial eff usion. J. Cardiovasc. Medю. (Hagerstown). 2019;20(1):39–45. DOI: 10.2459/JCM.0000000000000720
50. Bucher A.M., Henzel K., Meyer H.J., Ehrengut C., Müller L., Schramm D., Akinina A., Drechsel M., Kloeckner R., Isfort P., Sähn M.J., Fink M., More D., Melekh B., Meinel F.G., Dreger F., May M., Siegler L., Münzfeld H., Ruppel R., Penzkofer T., Kim M.S., Balzer M., Borggrefe J., Surov A. Pericardial Eff usion Predicts Clinical Outcomes in Patients with COVID-19: A Nationwide Multicenter Study. Acad. Radiol. 2024;31(5):1784–1791. DOI: 10.1016/j.acra.2023.12.003
51. Tsang T.S., Barnes M.E., Gersh B.J., Bailey K.R., Seward J.B. Outcomes of clinically signifi cant idiopathic pericardial eff usion requiring intervention. Am. J. Cardiol. 2003;91(6):704–7. DOI: 10.1016/s0002-9149(02)03408-2
52. Sukmarova Z.N., Simonenko V.B., Nasonov E.L. Treatment of patients with pericarditis with anti-inflammatory drugs. Clinical Medicine (Russian Journal). 2022;100(11–12):509–519. (In Russian)]. DOI: 10.30629/0023-2149-2022-100-11-12-509-519
53. Kim S.R., Kim E.K., Cho J., Chang S.A., Park S.J., Lee S.C., Park S.W. Eff ect of Anti-Infl ammatory Drugs on Clinical Outcomes in Patients With Malignant Pericardial Eff usion. J. Am. Coll. Cardiol. 2020;76(13):1551–1561. DOI: 10.1016/j.jacc.2020.08.003
54. Lazaros G., Antonopoulos AS., Lazarou E., Vlachopoulos C., Foukarakis E., Androulakis A., Manginas A., Theodoros K., Karavidas A., Tousoulis D. Long-Term Outcome of Pericardial Drainage in Cases of Chronic, Large, Hemodynamically Insignifi cant, C-Reactive Protein Negative, Idiopathic Pericardial Eff usions. Am. J. Cardiol. 2020;126:89–93. DOI: 10.1016/j.amjcard.2020.03.035
55. Virk S.A., Chandrakumar D., Villanueva C., Wolfenden H., Liou K., Cao C. Systematic review of percutaneous interventions for malignant pericardial eff usion. Heart. 2015;101:1619–1626. DOI: 10.1136/heartjnl-2015-307907
56. Kunitoh H., Tamura T., Shibata T., et al. A randomised trial of intrapericardial bleomycin for malignant pericardial eff usion with lung cancer (JCOG9811). Br. J. Cancer. 2009;100:464–469. DOI: 10.1038/sj.bjc.6604866
57. Saraç İ., Aydın S.Ş., Özmen M., Doru H.İ., Tonkaz G., Çırçır M.N., Akpınar F., Zengin O., Delice O., Aydınyılmaz F. Prevalence, Risk Factors, Prognosis, and Management of Pericardial Eff usion in COVID-19. J. Cardiovasc. Dev. Dis. 2023;10(9):ан368. DOI: 10.3390/jcdd10090368
58.
Review
For citations:
Sukmarova Z.N., Saidova M.A., Rybakova M.K. Pericardial effusion in coronavirus infection. Clinical Medicine (Russian Journal). 2025;103(4):249-262. (In Russ.) https://doi.org/10.30629/0023-2149-2025-103-4-249-262
Views:
18
Email this article 