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Патоморфологические и молекулярно-биологические аспекты повреждения кровеносных сосудов при COVID-19

https://doi.org/10.18499/2225-7357-2020-9-4-9-18

Аннотация

Коронавирусная инфекция COVID-19, вызванная SARS-CoV-2, связана не только с широким спектром респираторных синдромов, но и с выраженным деструктивным влиянием на кровеносные сосуды всего организма. Возраст и сопутствующая патология, предрасполагают к более тяжелому течению заболевания. В качестве общих неспецифических патоморфолологических изменений, развивающихся в кровеносных сосудах под влиянием SARS-CoV-2, можно выделить повреждение эндотелия, распространенные васкулиты и тромбозы. Для кровеносных сосудов легких помимо альтерации эндотелия и тромбоза был характерен ангиогенез по расщепляющему (инвагинационному) типу. Общим механизмом альтерации кровеносных сосудов и развития васкулопатий является прямое цитопатическое воздействие вируса на эндотелиоциты и иммуноопосредованное повреждение эндотелия, проявляющееся развитием эндотелиита, деструкцией межклеточных контактов эндотелиальных клеток, их набухаением и разобщением с базальной мембраной, сопровождающееся эндо- и периваскулярным воспалением. Молекулярно-биологические механизмы инвазии вируса вовлекают различные пути его проникновения в клетку и разнообразные формы развития воспалительного ответа с участием реакций врожденного и приобретенного иммунитета.

Об авторах

И. Э. Есауленко
ФГБОУ ВО «Воронежский государственный медицинский университет им. Н.Н. Бурденко» Минздрава России
Россия
Воронеж


Д. Б. Никитюк
ФГБУН «Федеральный исследовательский центр питания, биотехнологии и безопасности пищи»; ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России (Сеченовский университет)
Россия
Москва


Н. Т. Алексеева
ФГБОУ ВО «Воронежский государственный медицинский университет им. Н.Н. Бурденко» Минздрава России
Россия
Воронеж


А. А. Шевченко
БУЗ ВО «Воронежская городская клиническая больница скорой медицинской помощи №1»
Россия
Воронеж


Д. А. Соколов
ФГБОУ ВО «Воронежский государственный медицинский университет им. Н.Н. Бурденко» Минздрава России
Россия

Соколов Дмитрий Александрович

ул. Студенческая, 10, Воронеж, 394036



С. В. Клочкова
ФГАОУ ВО «Российский университет дружбы народов»; ГАУЗ «Московский научно-практический центр медицинской реабилитации, восстановительной и спортивной медицины ДЗМ»
Россия
Москва


А. Г. Кварацхелия
ФГБОУ ВО «Воронежский государственный медицинский университет им. Н.Н. Бурденко» Минздрава России
Россия
Воронеж


А. А. Филин
ФГБОУ ВО «Воронежский государственный медицинский университет им. Н.Н. Бурденко» Минздрава России
Россия
Воронеж


В. А. Тутельян
ФГБУН «Федеральный исследовательский центр питания, биотехнологии и безопасности пищи»
Россия
Москва


Список литературы

1. AbdelMassih AF, Kamel A, Mishriky F, Ismail H- A, El Qadi L, Malak L, et al. Is it infection or rather vascular inflammation? Game-changer insights and recommendations from patterns of multi-organ involvement and affected subgroups in COVID-19. Cardiovascular Endocrinology & Metabolism. 2020 Jun 11;9(3):110–20. doi: 10.1097/xce.0000000000000211

2. AbdelMassih AF, Ramzy D, Nathan L, Aziz S, Ashraf M, Youssef NH, et al. Possible molecular and paracrine involvement underlying the pathogenesis of COVID-19 cardiovascular complications. Cardiovascular Endocrinology & Metabolism. 2020 Apr 20;9(3):121–4. doi: 10.1097/xce.0000000000000207

3. Ackermann M, Stark H, Neubert L, Schubert S, Borchert P, Linz F, et al. Morphomolecular motifs of pulmonary neoangiogenesis in interstitial lung diseases. European Respiratory Journal. 2019 Dec 5;55(3):1900933. 10.1183/13993003.00933-2019

4. Ackermann M, Verleden SE, Kuehnel M, Haverich A, Welte T, Laenger F, et al. Pulmonary Vascular Endothelialitis, Thrombosis, and Angiogenesis in Covid-19. New England Journal of Medicine. 2020 May 21; doi: 10.1056/nejmoa2015432

5. Ahouach B, Harent S, Ullmer A, Martres P, Bégon E, Blum L, et al. Cutaneous lesions in a patient with COVID-19: are they related? British Journal of Dermatology. 2020 Jun 15;183(2). 10.1111/bjd.19168

6. Amor S, Fernández Blanco L, Baker D. Innate immunity during SARS-CoV-2: evasion strategies and activation trigger hypoxia and vascular damage. Clinical & Experimental Immunology. 2020 Sep 26; doi: 10.1111/cei.13523

7. Andersson U, Ottestad W, Tracey KJ. Extracellular HMGB1: a therapeutic target in severe pulmonary inflammation including COVID-19? Molecular Medicine. 2020 May 7;26(1). 10.1186/s10020-020-00172-4

8. Bangalore S, Sharma A, Slotwiner A, Yatskar L, Harari R, Shah B, et al. ST-Segment Elevation in Patients with Covid-19 — A Case Series. New England Journal of Medicine. 2020 Jun 18;382(25):2478–80. doi: 10.1056/nejmc2009020

9. Barton LM, Duval EJ, Stroberg E, Ghosh S, Mukhopadhyay S. COVID-19 Autopsies, Oklahoma, USA. American Journal of Clinical Pathology. 2020 Apr 10;(153):725–33. 10.1093/ajcp/aqaa062

10. Bhatia R, Pedapati R, Komakula S, Srivastava MVP, Vishnubhatla S, Khuranac D. Stroke in Coronavirus Disease 2019: A Systematic Review. Journal of Stroke. 2020 Sep 30;22(3):324–35. doi: 10.5853/jos.2020.02264

11. Bikdeli B, Madhavan MV, Jimenez D, Chuich T, Dreyfus I, Driggin E, et al. COVID-19 and Thrombotic or Thromboembolic Disease: Implications for Prevention, Antithrombotic Therapy, and Follow-up. Journal of the American College of Cardiology [Internet]. 2020 Apr 17;75(23). doi: 10.1016/j.jacc.2020.04.031

12. Booz GW, et al. Macrophage responses associated with COVID-19: A pharmacological perspective. European Journal of Pharmacology [Internet]. 2020 Nov 15 [cited 2020 Nov 8];887:173547. doi: 10.1016/j.ejphar.2020.173547

13. Bradley BT, Maioli H, Johnston R, Chaudhry I, Fink SL, Xu H, et al. Histopathology and ultrastructural findings of fatal COVID-19 infections in Washington State: a case series. The Lancet. 2020 Aug;396(10247):320–32. doi: 10.1016/s0140-6736(20)31305-2

14. Cai Y, Hao Z, Gao Y, Ping W, Wang Q, Peng S, et al. Coronavirus Disease 2019 in the Perioperative Period of Lung Resection: A Brief Report From a Single Thoracic Surgery Department in Wuhan, People’s Republic of China. Journal of Thoracic Oncology. 2020 Jun;15(6):1065–72. 10.1016/j.jtho.2020.04.003

15. Chen L, Li X, Chen M, Feng Y, Xiong C. The ACE2 expression in human heart indicates new potential mechanism of heart injury among patients infected with SARS-CoV-2. Cardiovascular Research. 2020 Mar 30;(116):1097–100. doi: 10.1093/cvr/cvaa078

16. Chen N, Zhou M, Dong X, Qu J, Gong F, Han Y, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. The Lancet [Internet]. 2020 Jan;395(10223). doi: 10.1016/s0140-6736(20)30211-7

17. Coperchini F, Chiovato L, Croce L, Magri F, Rotondi M. The Cytokine storm in COVID-19: An overview of the involvement of the chemokine/chemokine-receptor system. Cytokine & Growth Factor Reviews. 2020 May;(53):25–32. doi: 10.1016/j.cytogfr.2020.05.003

18. Coutard B, Valle C, de Lamballerie X, Canard B, Seidah NG, Decroly E. The spike glycoprotein of the new coronavirus 2019-nCoV contains a furin- like cleavage site absent in CoV of the same clade. Antiviral Research. 2020 Apr;176(176):104742. doi: 10.1016/j.antiviral.2020.104742

19. De Michele S, Sun Y, Yilmaz MM, Katsyv I, Salvatore M, Dzierba AL, et al. Forty Postmortem Examinations in COVID-19 Patients. American Journal of Clinical Pathology. 2020 Sep 2;154(6):748–60. doi: 10.1093/ajcp/aqaa156

20. Dimova I, Hlushchuk R, Makanya A, Styp-Rekowska B, Ceausu A, Flueckiger S, et al. Inhibition of Notch signaling induces extensive intussusceptive neo-angiogenesis by recruitment of mononuclear cells. Angiogenesis. 2013 Jul 24;16(4):921–37. 10.1007/s10456-013-9366-5

21. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, et al. A Novel Angiotensin-Converting Enzyme–Related Carboxypeptidase (ACE2) Converts Angiotensin I to Angiotensin 1-9. Circulation Research. 2000 Sep;87(5). 10.1161/01.res.87.5.e1

22. Durvasula R, Wellington T, McNamara E, Watnick S. COVID-19 and Kidney Failure in the Acute Care Setting: Our Experience From Seattle. American Journal of Kidney Diseases. 2020 Apr;(76). 10.1053/j.ajkd.2020.04.001

23. Fox SE, Akmatbekov A, Harbert JL, Li G, Quincy Brown J, Vander Heide RS. Pulmonary and cardiac pathology in African American patients with COVID-19: an autopsy series from New Orleans. The Lancet Respiratory Medicine. 2020 Jul;8(7):681–6. doi: 10.1016/s2213-2600(20)30243-5

24. Gianotti R, Veraldi S, Recalcati S, Cusini M, Ghislanzoni M, Boggio F, et al. Cutaneous Clinico-Pathological Findings in three COVID-19-Positive Patients Observed in the Metropolitan Area of Milan, Italy. Acta Dermato Venereologica. 2020;100(8):adv00124-2. 10.2340/00015555-3490

25. Hamming I, Timens W, Bulthuis M, Lely A, Navis G, van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. The Journal of Pathology. 2004 May 7;203(2):631–7.

26. Hanafi R, Roger P-A, Perin B, Kuchcinski G, Deleval N, Dallery F, et al. COVID-19 Neurologic Complication with CNS Vasculitis-Like Pattern. American Journal of Neuroradiology. 2020 Jun 18;41(8):1384–7. doi: 10.3174/ajnr.a6651

27. Hendren NS, Drazner MH, Bozkurt B, Cooper LT. Description and Proposed Management of the Acute COVID-19 Cardiovascular Syndrome. Circulation. 2020 Jun 9;141(23):1903–14. doi: 10.1161/circulationaha.120.047349

28. Herbst S, Schaible UE, Schneider BE. Interferon Gamma Activated Macrophages Kill Mycobacteria by Nitric Oxide Induced Apoptosis. Tailleux L, editor. PLoS ONE. 2011 May 2;6(5):e19105. doi: 10.1371/journal.pone.0019105

29. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. The Lancet [Internet]. 2020 Jan;395(10223). doi: 10.1016/s0140-6736(20)30183-5

30. Inciardi RM, Lupi L, Zaccone G, Italia L, Raffo M, Tomasoni D, et al. Cardiac Involvement in a Patient With Coronavirus Disease 2019 (COVID-19). JAMA Cardiology. 2020 Mar 27; doi: 10.1001/jamacardio.2020.1096

31. Juffroy O, Bugault F, Lambotte O, Landires I, Viard J-P, Niel L, et al. Dual Mechanism of Impairment of Interleukin-7 (IL-7) Responses in Human Immunodeficiency Virus Infection: Decreased IL-7 Binding and Abnormal Activation of the JAK/STAT5 Pathway. Journal of Virology. 2009 Oct 28;84(1):96–108. 10.1128/jvi.01475-09

32. Kadhim H, De Prez C, Gazagnes M-D, Sébire G. In situ cytokine immune responses in acute disseminated encephalomyelitis: Insights into pathophysiologic mechanisms. Human Pathology. 2003 Mar;34(3):293–7. 10.1053/hupa.2003.34

33. Kissling S, Rotman S, Gerber C, Halfon M, Lamoth F, Comte D, et al. Collapsing glomerulopathy in a COVID-19 patient. Kidney International [Internet]. 2020 Apr 15 [cited 2020 Jun 17];0(0). doi: 10.1016/j.kint.2020.04.006

34. Klok FA, Kruip MJHA, van der Meer NJM, Arbous MS, Gommers D, Kant KM, et al. Confirmation of the high cumulative incidence of thrombotic complications in critically ill ICU patients with COVID-19: An updated analysis. Thrombosis Research [Internet]. 2020 Apr 30 [cited 2020 May 24];191:148–50. doi: 10.1016/j.thromres.2020.04.041

35. Kolivras A, Dehavay F, Delplace D, Feoli F, Meiers I, Milone L, et al. Coronavirus (COVID-19) infection–induced chilblains: A case report with histopathologic findings. JAAD Case Reports. 2020 Jun;6(6):489–92. 10.1016/j.jdcr.2020.04.011

36. Konopka KE, Wilson A, Myers JL. Postmortem Lung Findings in an Asthmatic with Coronavirus Disease 2019 (COVID-19). Chest. 2020 Apr; 10.1016/j.chest.2020.04.032

37. Larsen CP, Bourne TD, Wilson JD, Saqqa O, Sharshir MA. Collapsing Glomerulopathy in a Patient With Coronavirus Disease 2019 (COVID-19). Kidney International Reports. 2020 Apr;(5):935–9.

38. Lee S, Meyler P, Mozel M, Tauh T, Merchant R. Asymptomatic carriage and transmission of SARS-CoV-2: What do we know? Canadian Journal of Anesthesia/Journal canadien d’anesth?sie. 2020 Jun 2;(67):1424–30. doi: 10.1007/s12630-020-01729-x

39. Li Y, Wang M, Zhou Y, Chang J, Xian Y, Mao L, et al. Acute Cerebrovascular Disease Following COVID-19: A Single Center, Retrospective, Observational Study. SSRN Electronic Journal. 2020; 10.2139/ssrn.3550025

40. Liu Q, Wang R, Qu G, Wang Y, Liu P, Zhu Y. Gross examination report of a COVID-19 death autopsy. Fa Yi Xue ZaZhi. 2020;(36):21–3.

41. Lovren F, Pan Y, Quan A, Teoh H, Wang G, Shukla PC, et al. Angiotensin converting enzyme-2 confers endothelial protection and attenuates atherosclerosis. American Journal of Physiology-Heart and Circulatory Physiology. 2008 Oct;295(4):H1377–84. doi: 10.1152/ajpheart.00331.2008

42. Lu R, Zhao X, Li J, Niu P, Yang B, Wu H, et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. The Lancet [Internet]. 2020 Jan;395(10224). doi: 10.1016/s0140-6736(20)30251-8

43. Magro C, Mulvey JJ, Berlin D, Nuovo G, Salvatore S, Harp J, et al. Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: a report of five cases. Translational Research. 2020 Apr; doi: 10.1016/j.trsl.2020.04.007

44. Menter T, Haslbauer JD, Nienhold R, Savic S, Hopfer H, Deigendesch N, et al. Post-mortem examination of COVID19 patients reveals diffuse alveolar damage with severe capillary congestion and variegated findings of lungs and other organs suggesting vascular dysfunction. Histopathology. 2020 May 4;77(2). doi: 10.1111/his.14134

45. Mondal R, Lahiri D, Deb S, Bandyopadhyay D, Shome G, Sarkar S, et al. COVID-19: Are we dealing with a multisystem vasculopathy in disguise of a viral infection? Journal of Thrombosis and Thrombolysis. 2020 Jul 5;50(3):567–79. doi: 10.1007/s11239-020-02210-8

46. Moutal A, Martin LF, Boinon L, Gomez K, Ran D, Zhou Y, et al. SARS-CoV-2 Spike protein co-opts VEGF-A/Neuropilin-1 receptor signaling to induce analgesia. bioRxiv. 2020 Jul 18; doi: 10.1101/2020.07.17.209288

47. Nieto-Torres JL, Verdiá-Báguena C, Jimenez-Guardeño JM, Regla-Nava JA, Castaño-Rodriguez C, Fernandez-Delgado R, et al. Severe acute respiratory syndrome coronavirus E protein transports calcium ions and activates the NLRP3 inflammasome. Virology. 2015 Nov;485:330–9. doi: 10.1016/j.virol.2015.08.010

48. Pangti R, Gupta S, Nischal N, Trikha A. Recognizable vascular skin manifestations of SARS CoV-2 infection are uncommon in patients with skin-of-color. Clinical and Experimental Dermatology. 2020 Aug 16; doi: 10.1111/ced.14421

49. Pernazza A, Mancini M, Rullo E, Bassi M, De Giacomo T, Rocca CD, et al. Early histologic findings of pulmonary SARS-CoV-2 infection detected in a surgical specimen. Virchows Archiv. 2020 Apr 30;1–6. doi: 10.1007/s00428-020-02829-1

50. Polak SB, Van Gool IC, Cohen D, von der Thüsen JH, van Paassen J. A systematic review of pathological findings in COVID-19: a pathophysiological timeline and possible mechanisms of disease progression. Modern Pathology [Internet]. 2020 Jun 22;1–11. doi: 10.1038/s41379-020-0603-3

51. Poor HD, Ventetuolo CE, Tolbert T, Chun G, Serrao G, Zeidman A, et al. COVID-9 critical illness pathophysiology driven by diffuse pulmonary thrombi and pulmonary endothelial dysfunction responsive to thrombolysis. Clinical and Translational Medicine. 2020 Jun;10(2). 10.1002/ctm2.44

52. Poyiadji N, Shahin G, Noujaim D, Stone M, Patel S, Griffith B. COVID-19–associated Acute Hemorrhagic Necrotizing Encephalopathy: CT and MRI Features. Radiology. 2020 Mar 31;201187. doi: 10.1148/radiol.2020201187

53. Rizzo P, Vieceli Dalla Sega F, Fortini F, Marracino L, Rapezzi C, Ferrari R. COVID-19 in the heart and the lungs: could we “Notch” the inflammatory storm? Basic Research in Cardiology. 2020 Apr 9;115(3). doi: 10.1007/s00395-020-0791-5

54. Schönrich G, Raftery MJ, Samstag Y. Devilishly radical NETwork in COVID-19: Oxidative stress, neutrophil extracellular traps (NETs), and T cell suppression. Advances in Biological Regulation. 2020 Aug;77:100741. 10.1016/j.jbior.2020.100741

55. Spiezia L, Boscolo A, Poletto F, Cerruti L, Tiberio I, Campello E, et al. COVID-19-Related Severe Hypercoagulability in Patients Admitted to Intensive Care Unit for Acute Respiratory Failure. Thrombosis and Haemostasis. 2020 Apr 21;4–6. doi: 10.1055/s-0040-1710018

56. Su H, Yang M, Wan C, Yi L-X, Tang F, Zhu H-Y, et al. Renal histopathological analysis of 26 postmortem findings of patients with COVID-19 in China. Kidney International [Internet]. 2020 Apr 9 [cited 2020 Apr 26];0(0). doi: 10.1016/j.kint.2020.04.003

57. Tavazzi G, Pellegrini C, Maurelli M, Belliato M, Sciutti F, Bottazzi A, et al. Myocardial localization of coronavirus in COVID-19 cardiogenic shock. European Journal of Heart Failure. 2020 Apr 11;22:911–5. doi: 10.1002/ejhf.1828

58. Tian S, Xiong Y, Liu H, Niu L, Guo J, Liao M, et al. Pathological study of the 2019 novel coronavirus disease (COVID-19) through postmortem core biopsies. Modern Pathology [Internet]. 2020 Apr 14 [cited 2020 Apr 21]; doi: 10.1038/s41379-020-0536-x

59. Varga Z, Flammer AJ, Steiger P, Haberecker M, Andermatt R, Zinkernagel AS, et al. Endothelial cell infection and endotheliitis in COVID-19. The Lancet [Internet]. 2020 Apr 21;395(10234). doi: 10.1016/S0140-6736(20)30937-5

60. Wichmann D. Autopsy Findings and Venous Thromboembolism in Patients With COVID-19. Annals of Internal Medicine. 2020 Dec 15;173(12):1030. doi: 10.7326/l20-1206

61. Xiong Y, Liu Y, Cao L, Wang D, Guo M, Guo D, et al. Transcriptomic Characteristics of Bronchoalveolar Lavage Fluid and Peripheral Blood Mononuclear Cells in COVID-19 Patients. SSRN Electronic Journal. 2020;(9):761–70. doi: 10.2139/ssrn.3549993

62. Xu Z, Shi L, Wang Y, Zhang J, Huang L, Zhang C, et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. The Lancet Respiratory Medicine [Internet]. 2020 Feb 18 [cited 2020 Mar 8];0(8):420–2. doi: 10.1016/S2213-2600(20)30076-X

63. Zamboni P. COVID-19 as a Vascular Disease: Lesson Learned from Imaging and Blood Biomarkers. Diagnostics. 2020 Jun 29;10(7):440. doi: 10.3390/diagnostics10070440

64. Zeng Z, Xu L, Xie X, Yan H, Xie B, Xu W, et al. Pulmonary pathology of early-phase COVID-19 pneumonia in a patient with a benign lung lesion. Histopathology. 2020 Sep 15; doi: 10.1111/his.14138

65. Zhu N, Zhang D, Wang W, Li X, Yang B, Song J, et al. A Novel Coronavirus from Patients with Pneumonia in China, 2019. New England Journal of Medicine. 2020 Jan 24;382(8). doi: 10.1056/nejmoa2001017


Рецензия

Для цитирования:


Есауленко И.Э., Никитюк Д.Б., Алексеева Н.Т., Шевченко А.А., Соколов Д.А., Клочкова С.В., Кварацхелия А.Г., Филин А.А., Тутельян В.А. Патоморфологические и молекулярно-биологические аспекты повреждения кровеносных сосудов при COVID-19. Журнал анатомии и гистопатологии. 2020;9(4):9-18. https://doi.org/10.18499/2225-7357-2020-9-4-9-18

For citation:


Esaulenko I.E., Nikityuk D.B., Alexeeva N.T., Shevchenko A.A., Sokolov D.A., Klochkova S.V., Kvaratskheliya A.G., Filin A.A., Tutel'yan V.A. Pathomorphological and Molecular Biological Aspects of Blood Vessel Injury in COVID-19. Journal of Anatomy and Histopathology. 2020;9(4):9-18. (In Russ.) https://doi.org/10.18499/2225-7357-2020-9-4-9-18

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