Lung lesions caused by COVID-19 in comparison with bacterial pneumonia and influenza pneumonia: pathomorphological features

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Abstract

This review aimed to summarize the literature data regarding the pathomorphology of lung lesions in COVID-19 and compare it with lung lesions in bacterial pneumonia and pneumonia caused by influenza virus. The analysis of scientific literature containing studies of domestic and foreign authors of different years related to morphology and anatomical pathology of lung injury was carried out. Special attention was paid to the data devoted to COVID-19 obtained between 2019 and 2021. Based on the study, the main aspects of lung lesions were identified and grouped into blocks depending on the etiology of the process. The review collects and summarizes information on etiology, pathogenesis and stages of disease development, outcomes and morphological picture during the autopsy of patients with bacterial pneumonia, influenza pneumonia and COVID-19 pneumonia. The common features and differences in the course, outcomes and typical morphological findings, most characteristics for each of the diseases were presented in the table. There is a great similarity of morphological findings in influenza pneumonia and COVID-19 pneumonia despite the background of the difference in their epidemiology. Most Russian and foreign authors agree that a key factor in the pathogenesis of the development of COVID-19 is the presence of a specific receptor-mediated pathway of penetration into the cells of the respiratory epithelium. According to most authors, the main morphological difference that determines the severity and unfavorable outcome of COVID-19 is angiopathy and microthrombosis of the pulmonary capillary bed, which aggravate the typical picture of viral pneumonia.

About the authors

R R Gainetdinov

Kazan (Volga Region) Federal University

Author for correspondence.
Email: asatrtinn@gmail.com
Russian Federation, Kazan, Russia

S V Kurochkin

City Clinical Hospital №7

Email: kurochkin.70@bk.ru

Cand. Sc. (Medicine), head of the Radiology-Diagnostic Department — radiologist, associate professor in Department of Fundamental Basis of Clinical Medicine
of KFU

Russian Federation, Kazan, Russia

References

  1. Sattar S.B.A., Sharma S. Bacterial pneumonia. Treasure Island (FL): StatPearls Publishing. 2020. https://www.ncbi.nlm.nih.gov/books/NBK513321/ (access date: 11.06.2021).
  2. Novikov V.E., Zubkov M.N., Gugutsidze E.N. Pneumococcal pneumonia in persons over 60 years of age: features of a specific humoral immune response. Pul'monologiya. 1991; (1): 15–19. (In Russ.)
  3. Zubkov M.N. Etiology and pathogenesis of community-acquired pneumonia in adults. Pul'monologiya. 2005; (5): 53–60. (In Russ.)
  4. Rachina S.A., Kozlov R.S., Shal E.P., Ustyuzhanin I.V., Krechikov O.I., Ivanchik N.V., Gudkov I.V., Asafyeva O.Yu., Guchev I.A., Gulyaeva S.A., Burdinskaya Yu.V., Yatsy­shina S.B., Astakhova T.S., Beykin Ya.B., Besedina L.G. A spectrum of causative bacterial pathogens in community-acquired pneumonia in multidisciplinary hospitals of smolensk. Pul'monologiya. 2011; (1): 5–18. (In Russ.)
  5. Golubev A.M., Smelaya T.V., Moroz V.V. Community-Acquired and Nosocomial Pneumonia: Clinical and Morphological Features. General reanimatology. 2010; 6 (3): 5–14. (In Russ.) doi: 10.15360/1813-9779-2010-3-5.
  6. Walker D.H. Chlamydial, mycoplasmal, rickettsial, and ehrlichial diseases. In: Pulmonary pathology. 2nd ed. Elsevier. 2018; 315–326. doi: 10.1016/B978-0-323-39308-9.00015-7.
  7. Jain V., Vashisht R., Yilmaz G., Bhardwaj A. Pneumonia pathology. Treasure Island (FL): StatPearls Publishing. 2020. https://www.ncbi.nlm.nih.gov/books/NBK526116/ (access date: 11.06.2021).
  8. Baranov A.A., Briko N.I., Namazova-Baranova L.S. Modern clinical and epidemiological characteristics of pneumococcal infections. Lechashchiy vrach. 2012; (4): 2–16. (In Russ.)
  9. Chernyaev A.L., Samsonova M.V. Pathological anatomy of pneumonia. Pul'monologiya i allergologiya. 2012; (4): 46–49. (In Russ.)
  10. Sinopal'nikov A.I. Respiratornaya meditsina. (Respiratory medicine.) Ed. by A.G. Chuchalina. Vol. 1. M.: GEOTAR-Media. 2007; 474–509. (In Russ.)
  11. Strukov A.I., Serov V.V. Patologicheskaya anatomiya. Uchebnik. (Pathological anatomy. Textbook.) 5th ed. M.: Litterra. 2010; 419–420. (In Russ.)
  12. Sattar S.B.A., Sharma S. Bacterial pneumonia. Treasure Island: StatPearls Publishing. 2021. PMID: 30020693.
  13. Kothe H., Bauer T., Marre R., Suttorp N., Welte T., Dalhoff K.; Competence Network for Community-Acquired Pneumonia study group. Outcome of community-acquired pneumonia: Influence of age, residence status and antimicrobial treatment. Eur. Resp. J. 2008; 32: 139–146. doi: 10.1183/09031936.00092507.
  14. Fine M.J., Stone R.A., Singer D.E., Coley C.M., Marrie T.J., Lave J.R., Hough L.J., Obrosky D.S., Schulz R., Ricci E.M., Rogers J.C., Kapoor W.N. Processes and outcomes of care for patients with community-acquired pneumonia: Results from the Pneumonia Patient Outcomes Research Team (PORT) Cohort Study. Arch. Intern. Med. 1999; 159 (9): 970–980. doi: 10.1001/archinte.159.9.970.
  15. Madani M.M., Jamieson S.W. Chronic thromboembolic pulmonary hypertension. Curr. Treat. Options. Cardiovasc. Med. 2000; 2: 141–148. doi: 10.1007/s11936-000-0007-0.
  16. Terrabuio A.A.Jr., Parra E.R., Farhat C., Cape­lozzi V.L. Autopsy-proven causes of death in lungs of patients immunocompromised by secondary interstitial pneumonia. Clinics. 2007; 62 (1): 69–76. doi: 10.1590/S1807-59322007000100011.
  17. Hespanhol V., Bárbara C. Pneumonia mortality, comorbidities matter? Pulmonology. 2020; 26 (3): 123–129. doi: 10.1016/j.pulmoe.2019.10.003.
  18. Juric G., Tentor D., Jakic-Razumovic J. Autopsy fin­dings and clinical diagnoses: retrospective study of 3,117 autopsies. Croat. Med. J. 1999; 40: 71–76. PMID: 9933899.
  19. Shieh W.J., Blau D.M., Denison A.M., Deleon-Carnes M., Adem P., Bhatnagar J., Sumner J., Liu L., Patel M., Batten B., Greer P., Jones T., Smith C., Bartlett J., Montague J., White E., Rollin D., Gao R., Seales C., Jost H., Metcalfe M., Goldsmith C.S., Humphrey C., Schmitz A., Drew C., Paddock C., Uyeki T.M., Zaki S.R. 2009 pandemic influenza A (H1N1): pathology and pathogenesis of 100 fatal cases in the United States. Am. J. Pathol. 2010; 177 (1): 166–175. doi: 10.2353/ajpath.2010.100115.
  20. Taubenberger J.K., Morens D.M. The patho­logy of influenza virus infections. Annu. Rev. Pathol. 2008; (3): 499–522. doi: 10.1146/annurev.pathmechdis.3.121806.154316.
  21. Basu A., Shelke V., Chadha M., Kadam D., Sangle S., Gangodkar S. Direct imaging of pH1N1 2009 influenza virus replication in alveolar pneumocytes in fatal cases by transmission electron microscopy. J. Electron Microscopy. 2011; 60 (1): 89–93. doi: 10.1093/jmicro/dfq081.
  22. Mulder J., Hers J.F.P. Influenza. Groningen: Wol­ters-Noordhoff. 1972; 287 р.
  23. Chartorizhskaya N.N., Sepp A.V., Prutkina E.V., Tsybikov N.N. Morphological characteristic of respiratory system affection at influenza a/h1n1 in Zabaikal region. Byulleten fiziologii i patologii dykhaniya. 2011; (39): 8–12. (In Russ.)
  24. Lynfield R., Davey R., Dwyer D.E., Losso M.H., Wentworth D., Cozzi-Lepri A., Herman-Lamin K., Cholewinska G., David D., Kuetter S., Ternesgen Z., Uyeki T., Lane H., Lundgren J., Neaton J. Outcomes of influenza A(H1N1)pdm09 virus infection: results from two international cohort studies. PLoS One. 2014; 9 (7): e101785. doi: 10.1371/journal.pone.0101785.
  25. Chernyaev A.L., Zajrat'yanc O.V., Polyanko N.I., Kelli E.I., Rogov K.A., Mihaleva L.M., Chartorizhskaya N.N., Trusov A.E., Samsonova M.V., Chuchalin A.G. Pathological anatomy of influenza A (Н1N1). Arkhiv patologii. 2010; (3): 3–6. (In Russ.)
  26. Chuchalin A.G., Chernyaev A.L., Zairatyants O.V., Kelly E.I., Rogov K.A., Mikhaleva L.M., Trusov A.E., Samsonova M.V., Charto­rizhskaya N.N. Pathological anatomy of the lungs in influenza A (H1N1) (autopsy data). Pul'monologiya. 2010 (1): 5–11. (In Russ.)
  27. Britto C.J., Brady V., Lee S., Dela Cruz C.S. Respiratory viral infections in chronic lung diseases. Clin. Chest Med. 2017; 38 (1): 87–96. doi: 10.1016/j.ccm.2016.11.014.
  28. Harms P.W., Schmidt L.A., Smith L.B., Newton D.W., Pletneva M.A., Walters L.L., Tomlins S.A., Fisher-Hubbard A., Napolitano L.M., Park P.K., Blaivas M., Fantone J., Myers J.L., Jentzen J.M. Autopsy fin­dings in eight patients with fatal H1N1 influenza. Am. J. Clin. Pathol. 2010; 134 (1): 27–35. doi: 10.1309/AJCP35KOZSAVNQZW.
  29. Gladkov S.A., Grigorieva I.V., Dedov V.A., Esaulenko E.V., Zinserling V.A. Clinicopathologic analysis of lethal influenza cases in 2009–2011. Zhurnal infektologii. 2011; 3 (4): 55–61. (In Russ.)
  30. Prasad H.B., Puranik S.C., Kadam D.B., Sangle S.A., Borse R.T., Basavraj A. Retrospective analysis of necropsy findings in patients of H1N1 and their correlation to clinical features. J. Assoc. Phys. India. 2011; 59: 498–500. PMID: 21887906.
  31. Chen G., Wu D., Guo W., Cao Y., Huang D., Wang H., Wang T., Zhang X., Chen H., Yu H., Zhang X., Zhang M., Wu S., Song J., Chen T., Han M., Li S., Luo X., Zhao J., Ning Q. Clinical and immunological features of severe and moderate coronavirus disease 2019. J. Clin. Invest. 2020; 130 (5): 2620–2629. doi: 10.1172/JCI137244.
  32. Zayrat'yants O.V., Samso­nova M.V., Mikhaleva L.M., Chernyaev A.L., Mishnev O.D., Krupnov N.M., Kalinin D.V. Patologicheskaya anatomiya COVID-19. Atlas. (Pathological anatomy of COVID-19. Atlas.) M.: DZM. 2020; 116 р. (In Russ.)
  33. Hamming I., Timens W., Bulthuis M.L., Lely A.T., Navis G., van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J. Pathol. 2004; 203 (2): 631–637. doi: 10.1002/path.1570.
  34. Chen T., Wu D., Chen H., Yan W., Yang D., Chen G., Ma K., Xu D., Yu H., Wang H., Wang T., Guo W., Chen J., Ding C., Zhang X., Huang J., Han M., Li S., Luo X., Zhao J., Ning Q. Clinical characteristics of 113 deceased patients with coronavirus disease 2019: retrospective study. BMJ. 2020; 368: m1091. doi: 10.1136/bmj.m1091.
  35. Chuchalin A.G. Interview with the ­scientific and practical journal “Pulmonology”. 2020. https://www.youtube.com/watch?v=qU-Ay92R6S0 (access date: 11.06.2021). (In Russ.)
  36. Yuki K., Jufiogi M., Koutsogiannaki S. COVID-19 pathophysiology: a review. Clin. Immunol. 2020; 215: 108427. doi: 10.1016/j.clim.2020.108427.
  37. Anguiano L., Riera M., Pascual J., Valdivielso J.M., Barrios C., Betriu A., Mojal S., Fernández E., So­ler M.J. NEFRONA study. Circulating angiotensin-converting enzyme 2 activity in patients with chronic kidney disease without previous history of cardiovascular disease. Nephrol. Dial. Transplant. 2015; 30 (7): 1176–1185. doi: 10.1093/ndt/gfv025.
  38. Barton L.M., Duval E.J., Stroberg E., Ghosh S., Mukhopadhyay S. COVID-19 autopsies, Oklahoma, USA. Am. J. Clin. Pathol. 2020; 153: 725–733. doi: 10.1093/ajcp/aqaa062.
  39. Xu Z., Shi L., Wang Y., Zhang J., Huang L., Zhang C., Liu S., Zhao P., Liu H., Zhu L., Tai Y., Bai C., Gao T., Song J., Xia P., Dong J., Zhao J., Wang F.S. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir. Med. 2020; 8: 420–422. doi: 10.1016/S2213-2600(20)30076-X.
  40. Zhang H., Zhou P., Wei Y., Yue H., Wang Y., Hu M., Zhang S., Cao T., Yang C., Li M., Guo G., Chen X., Chen Y., Lei M., Liu H., Zhao J., Peng P., Wang C.Y., Du R. Histopathologic changes and SARS-CoV-2 immunostai­ning in the lung of a patient with COVID-19. Ann. Inter. Med. 2020; 172: 629–632. doi: 10.7326/M20-0533.
  41. Magro C., Mulvey J.J., Berlin D., Nuovo G., Salvatore S., Harp J., Baxter-Stoltzfus A., Laurence J. Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: a report of five cases. Transl. Res. 2020; 220: 1–13. doi: 10.1016/j.trsl.2020.04.007.
  42. Su H., Yang M., Wan C., Yi L.X., Tang F., Zhu H.Y., Yi F., Yang H.C., Fogo A.B., Nie X., Zhang C. Renal histopathological analysis of 26 postmortem findings of patients with COVID-19 in China. Kidney Int. 2020; 98: 219–227. doi: 10.1016/j.kint.2020.04.003.
  43. Liu J., Zhang S., Wu Z., Shang Y., Dong X., Li G., Zhang L., Chen Y., Ye X., Du H., Liu Y., Wang T., Huang S., Chen L., Wen Z., Qu J., Chen D. Clinical outcomes of COVID-19 in Wuhan, China: a large cohort study. Ann. Intensive Care. 2020; 10: 99. doi: 10.1186/s13613-020-00706-3.
  44. Karagiannidis C., Mostert C., Hentschker C., Voshaar T., Malzahn J., Schillinger G., Klauber J., Janssens U., Marx G., Weber-Carstens S., Kluge S., Pfei­fer M., Grabenhenrich L., Welte T., Busse R. Case characteristics, resource use, and outcomes of 10 021 patients with COVID-19 admitted to 920 German hospitals: an observational study. Lancet Respir. Med. 2020; 8 (9): 853–862. doi: 10.1016/S2213-2600(20)30316-7.
  45. Borczuk A.C., Salvatore S.P., Seshan S.V., Patel S.S., Bussel J.B., Mostyka M., Elsoukkary S., He B., Del Vecchio C., Fortarezza F., Pezzuto F., Navalesi P., Crisanti A., Fowkes M.E., Bryce C.H., Calabrese F., Beasley M.B. COVID-19 pulmonary pathology: a multi-institutional autopsy cohort from Italy and New York City. Mod. Pathol. 2020; 33: 2156–2168. doi: 10.1038/s41379-020-00661-1.
  46. Malas M.B., Naazie I.N., Elsayed N., Mathlouthi A., Marmor R., Clary B. Thromboembolism risk of COVID-19 is high and associated with a higher risk of mortality: A systematic review and meta-analysis. Clin. Med. 2020; 29: 100639. doi: 10.1016/j.eclinm.2020.100639.
  47. Carsana L., Sonzogni A., Nasr A., Rossi R.S., Pellegrinelli A., Zerbi P., Rech R., Colombo R., Antinori S., Corbellino M., Galli M., Catena E., Tosoni A., Gianatti A., Nebuloni M. Pulmonary post-mortem findings in a series of COVID-19 cases from northern Italy: a two-centre descriptive study. Lancet Inf. Dis. 2020; 20 (10): 1135–1140. doi: 10.1016/S1473-3099(20)30434-5.
  48. Li G., Fox S.E., Summa B., Hu B., Wenk C., Akmatbekov A., Harbert J.L., Vander Heide R.S., Brown J.Q. Multiscale 3-dimensional pathology findings of COVID-19 di­seased lung using high-resolution cleared tissue microscopy. BioRxiv. 2020. doi: 10.1101/2020.04.11.037473.
  49. Duarte-Neto A.N., Monteiro R.A.A., da Silva L.F.F., Malheiros D.M.A.C., de Oliveira E.P., Theodoro-Filho J., Pinho J.R.R., Gomes-Gouvêa M.S., Salles A.P.M., de Oli­veira I.R.S., Mauad T., Saldiva P.H.N., Dolhnikoff M. Pulmonary and systemic involvement of COVID-19 assessed by ultrasound-guided minimally invasive autopsy. Histopathology. 2020; 77 (2): 186–197. doi: 10.1111/his.14160.
  50. Bradley B.T., Maioli H., Johnston R., Chaudhry I., Fink S.L., Xu H., Najafian B., Deutsch G., Lacy J.M., Williams T., Yarid N., Marshall D.A. Histopathology and ultrastructural findings of fatal COVID-19 infections in Wa­shington State: a case series. Lancet. 2020; 396: 320–332. doi: 10.1016/S0140-6736(20)31305-2.
  51. Grimes Z., Bryce C., Sordillo E.M., Gordon R.E., Reidy J., Paniz Mondolfi A.E., Fowkes M. Fatal pulmonary thromboembolism in SARS-CoV-2-infection. Cardiovasc. Pathol. 2020; 48: 107227. doi: 10.1016/j.carpath.2020.107227.
  52. Suess C., Hausmann R. Gross and histopathological pulmonary findings in a COVID-19 associated death during self-isolation. Int. J. Legal. Med. 2020; 134 (4): 1285–1290. doi: 10.1007/s00414-020-02319-8.
  53. Calabrese F., Pezzuto F., Fortarezza F., Hofman P., Kern I., Panizo A., von der Thüsen J., Timofeev S., Gor­kiewicz G., Lunardi F. Pulmonary pathology and COVID-19: lessons from autopsy. The experience of European Pulmonary Pathologists. Virchows Arch. 2020; 477: 359–372. doi: 10.1007/s00428-020-02886-6.
  54. Estimated influenza illnesses, medical visits, hospitalizations, and deaths in the United States — 2018–2019 influenza season. Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases (NCIRD). 2020. https://www.cdc.gov/flu/about/burden/2018-2019.html (access date: 11.06.2021).
  55. Meyerowitz-Katz G., Merone L. A ­systematic review and meta-analysis of published research data on COVID-19 infection fatality rates. Intern. J. Infect. Dis. 2020; 101: 138–148. doi: 10.1016/j.ijid.2020.09.1464.

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