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Long-term pathological changes in lungs after COVID-19

https://doi.org/10.18093/0869-0189-2021-31-5-571-579

Abstract

World literature is paying increasing attention to the long-term course of COVID-19 and symptoms that appear after the acute coronavirus infection. The symptoms, functional state of the lungs, and the X-ray changes are assessed. Nevertheless, post-COVID lung histology has not been described yet.

The aim of this article is to study the long-term pathological changes in the lungs after acute COVID-19. Methods. We analyzed autopsy lung material from 19 deceased who had COVID-19. The average age of the deceased was 68.82 ± 14.6 years. All patients were found to have IgG to SARS-CoV-2. The median time to death following viral interstitial pneumonia was 72 days. Results. The causes of death and thrombotic complications (infarctions of various organs and venous thrombosis) were analyzed. Histological examination revealed thrombosis of small pulmonary arteries and capillaries of interalveolar septa, microinfarctions, hemorrhages, foci of organizing pneumonia, and nonspecific interstitial pneumonia.

Conclusion. The first assessment of histological changes in human lungs showed that the most common post-COVID pathologic changes are microcirculation disorders combined with small areas of acute lung damage. The obtained data are essential for understanding the pathogenesis of post-COVID syndrome, necessitate diagnostic of microvasculature disorders using laboratory tests, scintigraphy, and CT imaging, as well as search for the therapeutic strategies.

About the Authors

Maria V. Samsonova
Federal Pulmonology Research Institute, Federal Medical and Biological Agency; A.S.Loginov Moscow State Clinical and Research Center, Moscow Healthcare Department
Russian Federation

Maria V. Samsonova, Doctor of Medicine, Head of the Pathology Department; Senior Researcher, Laboratory of Pathomorphology

Orekhovyy bul’var 28, Moscow, 115682;

Shosse Entuziastov 86, Moscow, 111123

tel.: (495) 465-58-59


Competing Interests:

The authors declare no conflict of interest



Andrey S. Kontorschikov
Federal State Budgetary Institution “A.P. Avtsyn Research Institute of Human Morphology”
Russian Federation

Andrey S. Kontorschikov, Clinical Morphology Laboratory Resident

ul. Tsyurupy 3, Moscow, 117418

tel.: (499) 120-80-65


Competing Interests:

The authors declare no conflict of interest



Andrey L. Cherniaev
Federal Pulmonology Research Institute, Federal Medical and Biological Agency; Federal State Budgetary Institution “A.P. Avtsyn Research Institute of Human Morphology”; Pirogov Russian National Research Medical University (Pirogov Medical University), Healthcare Ministry
Russian Federation

Andrey L. Cherniaev, Doctor of Medicine, Head of the Department of Fundamental Pulmonology; Laboratory of Clinical Morphology; Professor of the Department of Pathological Anatomy and Clinical Pathological Anatomy, Faculty of Medicine

Orekhovyy bul’var 28, Moscow, 115682;

ul. Tsyurupy 3, Moscow, 117418;

ul. Ostrovityanova 1, Moscow, 117997

tel.: (495) 465-58-59


Competing Interests:

The authors declare no conflict of interest



Kirill Yu. Mikhajlichenko
Federal Pulmonology Research Institute, Federal Medical and Biological Agency
Russian Federation

Kirill Yu. Mikhajlichenko, Researcher, Pathology Department

Orekhovyy bul’var 28, Moscow, 115682

tel.: (495) 465-58-59


Competing Interests:

The authors declare no conflict of interest



Liudmila M. Mikhaleva
Federal State Budgetary Institution “A.P. Avtsyn Research Institute of Human Morphology”
Russian Federation

Liudmila M. Mikhaleva, Doctor of Medicine, Professor, Director, Head of the Clinical Morphology Laboratory

ul. Tsyurupy 3, Moscow, 117418

tel.: (499) 120-80-65


Competing Interests:

The authors declare no conflict of interest



Oleko D. Mishnev
Pirogov Russian National Research Medical University (Pirogov Medical University), Healthcare Ministry
Russian Federation

Oleko D. Mishnev, Doctor of Medicine, Professor, Head of the Department of Pathological Anatomy and Clinical Pathological Anatomy, Faculty of Medicine

ul. Ostrovityanova 1, Moscow, 117997

tel.: (495) 434-03-29


Competing Interests:

The authors declare no conflict of interest



Oleg V. Zayratyants
Federal State Budgetary Institution “A.P. Avtsyn Research Institute of Human Morphology”; A.I. Yevdokimov Moscow State University of Medicine and Dentistry, Healthcare Ministry
Russian Federation

Oleg V. Zayratyants, Doctor of Medicine, Professor, Leading Researcher; Head of the Department of Pathological Anatomy

SPIN: 4817-1084

ul. Tsyurupy 3, Moscow, 117418;

ul. Delegatskaya 20/1, Moscow, 127473

tel.: (495) 609-22-50


Competing Interests:

The authors declare no conflict of interest



References

1. World Health Organization. A coordinated Global Research Roadmap. 2019 novel coronavirus. Global research and innovation forum: towards a research roadmap. Available at: https://www.who.int/blueprint/priority-diseases/key-action/Roadmap-version-FINAL-for-WEB.pdf?ua=1

2. Pavli A., Theodoridou M., Maltezou H.C. Post-COVID syndrome: Incidence, clinical spectrum, and challenges for primary healthcare professionals. Arch. Med. Res. 2021; 52 (6): 575–581. DOI: 10.1016/j.arcmed.2021.03.010.

3. Havervall S., Rosell A., Phillipson M. et al. Symptoms and functional impairment assessed 8 months after mild COVID-19 among health care workers. JAMA. 2021. 325 (19): 2015–2016. DOI: 10.1001/jama.2021.5612.

4. Moreno-Perez O., Merino E., Leon-Ramirez J.M. et al. Post-acute COVID-19 syndrome. Incidence and risk factors: A Mediterranean cohort study. J. Infect. 2021; 82 (3) 373–378. DOI: 10.1016/j.jinf.2021.01.004.

5. Patient-Led Research Collaborative. Report: What Does COVID-19 Recovery Actually Look Like? An Analysis of the Prolonged COVID-19 Symptoms Survey by Patient-Led Research Team. Available at: https://patientresearchcovid19.com/research/report-1/ [Accessed: 7 May, 2021].

6. Maltezou H.C., Raftopoulos V., Vorou R. et al. Association between upper respiratory tract viral load, comorbidities, disease severity, and outcome of patients with SARS-CoV-2 infection. J. Infect. Dis. 2021; 223 (7): 1132–1138. DOI: 10.1093/infdis/jiaa804.

7. Machado F.V.C., Meys R., Delbressine J.M. et al. Construct validity of the Post-COVID-19 Functional Status Scale in adult subjects with COVID-19. Health Qual Life Outcomes. 2021; 19 (1): 40. DOI: 10.1186/s12955-021-01691-2.

8. Garg P., Arora U., Kumar A., Wig N. The “post-COVID” syndrome: How deep is the damage? J. Med. Virol. 2021; 93 (2): 673–674. DOI: 10.1002/jmv.26465.

9. McDonald L.T. Healing after COVID-19: are survivors at risk for pulmonary fibrosis? Am. J. Physiol. Lung Cell. Mol. Physiol. 2021; 320 (2): L257–265. DOI: 10.1152/ajplung.00238.2020.

10. Ostergaard L. SARS CoV-2 related microvascular damage and symptoms during and after COVID-19: Consequences of capillary transit-time changes, tissue hypoxia and inflammation. Physiol. Rep. 2021; 9 (3): e14726. DOI: 10.14814/phy2.14726.

11. Wagner W.L., Hellbach K., Fiedler M.O. et al. [Microvascular changes in COVID-19]. Radiologe. 2020; 60 (10): 934–942. DOI: 10.1007/s00117-020-00743-w (in German).

12. Eapen M.S., Lu W., Gaikwad A.V. et al. Endothelial to mesenchymal transition: a precursor to post-COVID-19 interstitial pulmonary fibrosis and vascular obliteration? Eur. Respir. J. 2020; 56 (4): 2003167. DOI: 10.1183/13993003.03167-2020.

13. Samsonova M.V., Chernyaev A.L., Omarova Zh.R. et al. [Features of pathological anatomy of lungs at COVID-19]. Pulmonologiya. 2020; 30 (5): 519–532. DOI: 10.18093/0869-0189-2020-30-5-519-532 (in Russian).

14. Li Y., Wu J., Wang S. et al. Progression to fibrosing diffuse alveolar damage in a series of 30 minimally invasive autopsies with COVID-19 pneumonia in Wuhan, China. Histopathology. 2021, 78 (4), 542–555. DOI: 10.1111/his.14249.

15. Deshmukh V., Motwani R., Kumar A. et al. Histopathological observations in COVID-19: a systematic review. J. Clin. Pathol. 2021; 74 (2): 76–83. DOI: 10.1136/jclinpath-2020-206995.

16. Ali R.M.M., Ghonimy M.B.I. Post-COVID-19 pneumonia lung fibrosis: a worrisome sequelae in surviving patients. Egypt. J. Radiol. Nucl. Med. 2021; 52: 101. DOI: 10.1186/s43055-021-00484-3.

17. Avdeev S.N., Karchevskaya N.A., Baimakanova G.E., Cherniak A.V. [A one-year follow-up study of patients survived after ALI/ARDS caused by influenza A/H1N1]. Pul’monologiya. 2011; (4): 58–66. DOI: 10.18093/0869-0189-2011-0-4-58-66 (in Russian).

18. Xie L., Liu Y., Fan B. et al. Dynamic changes of serum SARS-coronavirus IgG, pulmonary function and radiography in patients recovering from SARS after hospital discharge. Respir. Res. 2005; 6 (1): 5. DOI: 10.1186/1465-9921-6-5.

19. Schaller T., Hirschbühl K., Burkhardt K. et al. Postmortem examination of patients with COVID-19. JAMA. 2020; 323 (24): 2518–2520. DOI: 10.1001/jama.2020.8907.

20. Townsend L., Fogarty H., Dyer A. et al. Prolonged elevation of D-dimer levels in convalescent COVID-19 patients is independent of the acute phase response. J. Thromb. Haemost. 2021; 19 (4): 1064–1070. DOI: 10.1111/jth.15267.

21. Torres-Castro R., Vasconcello-Castilloa L., Alsina-Restoy X. et al. Respiratory function in patients post-infection by COVID-19: a systematic review and meta-analysis. Pulmonology. 2021; 27 (4): 328–327. DOI: 10.1016/j.pulmoe.2020.10.013.

22. So M., Kabata H., Fukunaga K. et al. Radiological and functional lung sequelae of COVID-19: a systematic review and meta-analysis. BMC Pulm. Med. 2021; 21 (1): 97. DOI: 10.1186/s12890-021-01463-0.

23. Bellan M, Soddu D., Balbo P.E. et al. Respiratory and psychophysical sequelae among patients with COVID-19 four months after hospital discharge. JAMA Netw. Open. 2021; 4 (1): e2036142. DOI: 10.1001/jamanetworkopen.2020.36142.

24. Savushkina O.I., Chernyak A.V., Kryukov E.V. et al. [Pulmonary function after COVID-19 in early convalescence phase]. Meditsinskiy alfavit. 2020; (25): 7–12. DOI: 10.33667/2078-5631-2020-25-7-12 (in Russian).

25. Zhao Y.M., Shang Y.M., Song W.B. et al. Follow-up study of the pulmonary function and related physiological characteristics of COVID-19 survivors three months after recovery. EClinicalMedicine. 2020; 25: 100463. DOI: 10.1016/j.eclinm.2020.100463.

26. Kumar M.A., Krishnaswamy M., Arul J.N. Post COVID-19 sequelae: venous thromboembolism complicated by lower GI bleed. BMJ Case Rep. 2021; 14 (1): e241059. DOI: 10.1136/bcr-2020-241059.

27. Patelli G., Paganoni S., Besana F. et al. Preliminary detection of lung hypoperfusion in discharged Covid-19 patients during recovery. Eur. J. Radiol. 2020; 129: 109121. DOI: 10.1016%2Fj.ejrad.2020.109121.

28. Dhawan R.T., Gopalan D., Howard L. et al. Beyond the clot: perfusion imaging of the pulmonary vasculature after COVID-19. Lancet Res. Med. 2021; 9 (1): 107–116. DOI: 10.1016/S2213-2600(20)30407-0.

29. Remy-Jardin M., Duthoit L., Perez T. et al. Assessment of pulmonary arterial circulation 3 months after hospitalization for SARSCoV- 2 pneumonia: Dual-energy CT (DECT) angiographic study in 55 patients. EClinicalMedicine. 2021; 34: 100778. DOI: 10.1016/j.eclinm.2021.100778.

30. Morris S.B., Schwartz N.G., Patel P. et al. Case series of multisystem inflammatory syndrome in adults associated with SARS-CoV-2 infection – United Kingdom and United States, March–August 2020. MMWR Morb. Mortal. Wkly Rep. 2020; 69 (40): 1450–1456. DOI: 10.15585/mmwr.mm6940e1.

31. Galstyan G.M. [Coagulopathy in COVID-19]. Pul’monologiya. 2020; 30 (5): 645–657. DOI: 10.18093/0869-0189-2020-30-5-645-657 (in Russian).

32. Brodard J., Kremer Hovinga J.A., Fontana P. et al. COVID-19 patients often show high-titer non-platelet-activating anti-PF4/heparin IgG antibodies. J. Thromb. Haemost. 2021; 19 (5): 1294–1298. DOI: 10.1111/jth.15262.

33. Pretorius E., Vlok M., Venter C. et al. Persistent clotting protein pathology in long COVID/Post-Acute Sequelae of COVID-19 (PASC) is accompanied by increased levels of antiplasmin. Cardiovasc. Diabetol. 2021; 20 (1): 172. DOI: 10.1186/s12933-021-01359-7.

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Review

For citations:


Samsonova M.V., Kontorschikov A.S., Cherniaev A.L., Mikhajlichenko K.Yu., Mikhaleva L.M., Mishnev O.D., Zayratyants O.V. Long-term pathological changes in lungs after COVID-19. PULMONOLOGIYA. 2021;31(5):571-579. (In Russ.) https://doi.org/10.18093/0869-0189-2021-31-5-571-579

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ISSN 0869-0189 (Print)
ISSN 2541-9617 (Online)