Clinical and morphological features of lung injury long-term after SARS-CoV-2 recovery
- 作者: Baimakanova G.1, Samsonova M.1,2, Chernyaev A.2,3,4, Kontorschikov A.3, Belevskiy A.4
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隶属关系:
- Loginov Moscow Clinical Scientific Center
- Research Institute of Pulmonology
- Petrovsky National Research Centre of Surgery
- Pirogov Russian National Research Medical University
- 期: 卷 96, 编号 3 (2024)
- 页面: 218-227
- 栏目: Original articles
- URL: https://journals.rcsi.science/0040-3660/article/view/255126
- DOI: https://doi.org/10.26442/00403660.2024.03.202647
- ID: 255126
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详细
Aim. To study the clinical and histological profile of lung tissue in patients with persistent pulmonary disease, respiratory symptoms and CT findings after SARS-CoV-2 infection.
Materials and methods. The study included 15 patients (7 females and 8 males) with a mean age of 57.7 years. All patients underwent laboratory tests, chest computed tomography, echocardiography, and pulmonary function tests. Pulmonary tissue and bronchoalveolar lavage samples were obtained by fibrobronchoscopy, transbronchial forceps (2 patients), and lung cryobiopsy (11 patients); open biopsy was performed in 2 patients. Cellular composition, herpesvirus DNA, SARS-CoV-2, Mycobacterium tuberculosis complex, galactomannan optical density index, and bacterial and fungal microflora growth were determined in bronchoalveolar lavage. SARS-CoV-2 was also identified in samples from the nasal mucosa, throat and feces using a polymerase chain reaction.
Results. The results showed no true pulmonary fibrosis in patients recovered from SARS-CoV-2 infection with persistent respiratory symptoms, functional impairment, and CT findings after SARS-CoV-2 infection. The observed changes comply with the current and/or resolving infection and inflammatory process.
Conclusion. Thus, no true pulmonary fibrosis was found in patients after SARS-CoV-2 infection with persistent respiratory symptoms, functional impairment, and CT findings. The observed changes comply with the current and/or resolving infection and inflammatory process.
作者简介
Gulsara Baimakanova
Loginov Moscow Clinical Scientific Center
编辑信件的主要联系方式.
Email: g.baymakanova@mknc.ru
ORCID iD: 0000-0001-8198-9313
д-р мед. наук, зав. отд. пульмонологии ГБУЗ «МКНЦ им. А.С. Логинова»
俄罗斯联邦, MoscowMaria Samsonova
Loginov Moscow Clinical Scientific Center; Research Institute of Pulmonology
Email: samary@mail.ru
ORCID iD: 0000-0001-8170-1260
д-р мед. наук, ст. науч. сотр. лаб. патоморфологии ГБУЗ «МКНЦ им. А.С. Логинова», зав. лаб. патологической анатомии ФГБУ «НИИ пульмонологии»
俄罗斯联邦, Moscow; MoscowAndrey Chernyaev
Research Institute of Pulmonology; Petrovsky National Research Centre of Surgery; Pirogov Russian National Research Medical University
Email: cheral12@gmail.com
ORCID iD: 0000-0002-0158-7056
д-р мед. наук, проф., зав. отд. фундаментальной пульмонологии ФГБУ «НИИ пульмонологии», вед. науч. сотр. НИИМЧ им. акад. А.П. Авцына ФГБНУ «РНЦХ им. акад. Б.В. Петровского», проф. каф. патологической анатомии и клинической патологической анатомии лечебного фак-та ФГАОУ ВО «РНИМУ им. Н.И. Пирогова»
俄罗斯联邦, Moscow; Moscow; MoscowAndrey Kontorschikov
Petrovsky National Research Centre of Surgery
Email: g.baymakanova@mknc.ru
ORCID iD: 0000-0002-1032-0353
ординатор лаб. клинической морфологии НИИМЧ им. акад. А.П. Авцына ФГБНУ «РНЦХ им. акад. Б.В. Петровского»
俄罗斯联邦, MoscowAndrey Belevskiy
Pirogov Russian National Research Medical University
Email: pulmobas@yandex.ru
ORCID iD: 0000-0001-6050-724X
д-р мед. наук, проф., зав. каф. пульмонологии ФГАОУ ВО «РНИМУ им. Н.И. Пирогова», президент Российского респираторного общества, гл. внештатный специалист – пульмонолог Департамента здравоохранения г. Москвы
俄罗斯联邦, Moscow参考
- WHO. WHO coronavirus disease (COVID-19) dashboard. Available at: https://data.who.int/dashboards/covid19/cases?n=c. Accessed: 14.12.2023.
- Soriano JB, Murthy S, Marshall JC, et al. WHO Clinical Case Definition Working Group on Post-COVID-19 Condition. A clinical case definition of post-COVID-19 condition by a Delphi consensus. Lancet Infect Dis. 2022;22(4):e102-7. doi: 10.1016/S1473-3099(21)00703-9
- Чучалин А.Г. COVID-19 и безопасность человека. Терапевтический архив. 2021;93(3):253-4 [Chuchalin AG. COVID-19 and human safety. Terapevticheskii Arkhiv (Ter. Arkh.). 2021;93(3):253-4 (in Russian)]. doi: 10.26442/00403660.2021.03.200717
- Лизинфельд И.А., Пшеничная Н.Ю., Паролина Л.Е., и др. Оценка факторов, влияющих на вероятность госпитализации больных COVID-19 с сопутствующей патологией, и разработка на их основе прогностической модели. Терапевтический архив. 2022;94(1):57-63 [Lizinfeld IA, Pshenichnaya NYu, Parolina LE, et al. Assessing factors influencing the likelihood of hospitalization of COVID-19 patients with concomitant pathologies and developing a prognostic model based on them. Terapevticheskii Arkhiv (Ter. Arkh.). 2022;94(1):57-63 (in Russian)]. doi: 10.26442/00403660.2022.01.201323
- Чучалин А.Г. Фиброз легких у больных, перенесших COVID-19. Терапевтический архив. 2022;94(11):1333-9 [Chuchalin AG. Pulmonary fibrosis in patients who have had COVID-19. Terapevticheskii Arkhiv (Ter. Arkh.). 2022;94(11):1333-9 (in Russian)]. doi: 10.26442/00403660.2022.11.201943
- Авдеев С.Н., Адамян Л.В., Алексеева Е.И., и др. Профилактика, диагностика и лечение новой коронавирусной инфекции (COVID-19): временные методические рекомендации. Версия 15 (22.02.2022). М. 2022 [Avdeiev SN, Adamian LV, Alekseeva EI, et al. Profilaktika, diagnostika i lecheniie novoi koronavirusnoi infektsii (COVID-19): vremennyie metodicheskiie rekomendatsii. Versiia 15 (22.02.2022). Moscow. 2022 (in Russian)].
- Маннанова И.В., Семенов В.Т., Понежева Ж.Б., и др. Клинико-лабораторная характеристика COVID-19. РМЖ. 2021;4:22-5 [Mannanova IV, Semenov VT, Ponezheva ZhB, et al. Clinical and laboratory characteristics of COVID-19. RMJ. 2021;4:22-5 (in Russian)].
- Малеев В.В., Вединов С.М., Городин В.Н. Современные представления о церебральной дисфункции при COVID-19. Инфекционные болезни. 2021;19(3):109-15 [Maleev VV, Vedinov SM, Gorodin VN. Modern concepts of cerebral dysfunction at COVID-19. Infectious Diseases. 2021;19(3):109-15 (in Russian)]. doi: 10.20953/1729-9225-2021-3-109-115
- Seeßle J, Waterboer T, Hippchen T, et al. Persistent Symptoms in Adult Patients 1 Year After Coronavirus Disease 2019 (COVID-19): A Prospective Cohort Study. Clin Infect Dis. 2022;74(7):1191-8. doi: 10.1093/cid/ciab611
- Rivera-Izquierdo M, Láinez-Ramos-Bossini AJ, de Alba IG, et al. Long COVID 12 months after discharge: persistent symptoms in patients hospitalised due to COVID-19 and patients hospitalised due to other causes – a multicentre cohort study. BMC Med. 2022;20(1):92. doi: 10.1186/s12916-022-02292-6
- Liu T, Wu D, Yan W, et al. Twelve-Month Systemic Consequences of Coronavirus Disease 2019 (COVID-19) in Patients Discharged From Hospital: A Prospective Cohort Study in Wuhan, China. Clin Infect Dis. 2022;74(11):1953-65. doi: 10.1093/cid/ciab703
- Huang L, Li X, Gu X, et al. Health outcomes in people 2 years after surviving hospitalisation with COVID-19: a longitudinal cohort study. Lancet Respir Med. 2022;10(9):863-76. doi: 10.1016/S2213-2600(22)00126-6
- Chen Y, Ding C, Yu L, et al. One-year follow-up of chest CT findings in patients after SARS-CoV-2 infection. BMC Med. 2021;19(1):191. doi: 10.1186/s12916-021-02056-8
- Han X, Fan Y, Alwalid O, et al. Fibrotic Interstitial Lung Abnormalities at 1-year Follow-up CT after Severe COVID-19. Radiology. 2021;301(3):E438-40. doi: 10.1148/radiol.2021210972
- Pan F, Yang L, Liang B, et al. Chest CT Patterns from Diagnosis to 1 Year of Follow-up in Patients with COVID-19. Radiology. 2022;302(3):709-19. doi: 10.1148/radiol.2021211199
- Luger AK, Sonnweber T, Gruber L, et al. Chest CT of Lung Injury 1 Year after COVID-19 Pneumonia: The CovILD Study. Radiology. 2022;304(2):462-70. doi: 10.1148/radiol.211670
- Eberst G, Claudé F, Laurent L, et al. Result of one-year, prospective follow-up of intensive care unit survivors after SARS-CoV-2 pneumonia. Ann Intensive Care. 2022;12(1):23. doi: 10.1186/s13613-022-00997-8
- Vijayakumar B, Tonkin J, Devaraj A, et al. CT Lung Abnormalities after COVID-19 at 3 Months and 1 Year after Hospital Discharge. Radiology. 2022;303(2):444-54. doi: 10.1148/radiol.2021211746
- Bocchino M, Lieto R, Romano F, et al. Chest CT-based Assessment of 1-year Outcomes after Moderate COVID-19 Pneumonia. Radiology. 2022;305(2):479-85. doi: 10.1148/radiol.220019
- Guler SA, Ebner L, Aubry-Beigelman C, et al. Pulmonary function and radiological features 4 months after COVID-19: first results from the national prospective observational Swiss COVID-19 lung study. Eur Respir J. 2021;57(4):2003690. doi: 10.1183/13993003.03690-2020
- van Gassel RJJ, Bels JLM, Raafs A, et al. High Prevalence of Pulmonary Sequelae at 3 Months after Hospital Discharge in Mechanically Ventilated Survivors of COVID-19. Am J Respir Crit Care Med. 2021;203(3):371-4. doi: 10.1164/rccm.202010-3823LE
- Caruso D, Guido G, Zerunian M, et al. Post-Acute Sequelae of COVID-19 Pneumonia: Six-month Chest CT Follow-up. Radiology. 2021;301(2):E396-405. doi: 10.1148/radiol.2021210834
- Ravaglia C, Doglioni C, Chilosi M, et al. Clinical, radiological and pathological findings in patients with persistent lung disease following SARS-CoV-2 infection. Eur Respir J. 2022;60(4):2102411. doi: 10.1183/13993003.02411-2021
- Aesif SW, Bribriesco AC, Yadav R, et al. Pulmonary Pathology of COVID-19 Following 8 Weeks to 4 Months of Severe Disease: A Report of Three Cases, Including One With Bilateral Lung Transplantation. Am J Clin Pathol. 2021;155(4):506-14. doi: 10.1093/ajcp/aqaa264
- Konopka KE, Perry W, Huang T, et al. Usual Interstitial Pneumonia is the Most Common Finding in Surgical Lung Biopsies from Patients with Persistent Interstitial Lung Disease Following Infection with SARS-CoV-2. EClinicalMedicine. 2021;42:101209. doi: 10.1016/j.eclinm.2021.101209
- Swank Z, Senussi Y, Manickas-Hill Z, et al. Persistent Circulating Severe Acute Respiratory Syndrome Coronavirus 2 Spike Is Associated With Post-acute Coronavirus Disease 2019 Sequelae. Clin Infect Dis. 2023;76(3):e487-90. doi: 10.1093/cid/ciac722
- Proal AD, VanElzakker MB. Long COVID or Post-acute Sequelae of COVID-19 (PASC): An Overview of Biological Factors That May Contribute to Persistent Symptoms. Front Microbiol. 2021;12:698169. doi: 10.3389/fmicb.2021.698169
- Phetsouphanh C, Darley DR, Wilson DB, et al. Immunological dysfunction persists for 8 months following initial mild-to-moderate SARS-CoV-2 infection. Nat Immunol. 2022;23(2):210-6. doi: 10.1038/s41590-021-01113-x
- Zubchenko S, Kril I, Nadizhko O, et al. Herpesvirus infections and post-COVID-19 manifestations: a pilot observational study. Rheumatol Int. 2022;42(9):1523-30. doi: 10.1007/s00296-022-05146-9
- Liu Q, Mak JWY, Su Q, et al. Gut microbiota dynamics in a prospective cohort of patients with post-acute COVID-19 syndrome. Gut. 2022;71(3):544-52. doi: 10.1136/gutjnl-2021-325989
- Yeoh YK, Zuo T, Lui GC, et al. Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19. Gut. 2021;70(4):698-706. doi: 10.1136/gutjnl-2020-323020
- Wallukat G, Hohberger B, Wenzel K, et al. Functional autoantibodies against G-protein coupled receptors in patients with persistent Long-COVID-19 symptoms. J Transl Autoimmun. 2021;4:100100. doi: 10.1016/j.jtauto.2021.100100
- Su Y, Yuan D, Chen DG, et al. Multiple early factors anticipate post-acute COVID-19 sequelae. Cell. 2022;185(5):881-95.e20. doi: 10.1016/j.cell.2022.01.014
- Arthur JM, Forrest JC, Boehme KW, et al. Development of ACE2 autoantibodies after SARS-CoV-2 infection. PLoS One. 2021;16(9):e0257016. doi: 10.1371/journal.pone.0257016
- Charfeddine S, Ibn Hadj Amor H, Jdidi J, et al. Long COVID-19 Syndrome: Is It Related to Microcirculation and Endothelial Dysfunction? Insights From TUN-EndCOV Study. Front Cardiovasc Med. 2021;8:745758. doi: 10.3389/fcvm.2021.745758
- Pretorius E, Venter C, Laubscher GJ, et al. Prevalence of symptoms, comorbidities, fibrin amyloid microclots and platelet pathology in individuals with Long COVID/Post-Acute Sequelae of COVID-19 (PASC). Cardiovasc Diabetol. 2022;21(1):148. doi: 10.1186/s12933-022-01579-5
- Spudich S, Nath A. Nervous system consequences of COVID-19. Science. 2022;375(6578):267-9. doi: 10.1126/science.abm2052
- Ehab A, Reissfelder F, Laufer J, et al. Transbronchial lung cryobiopsy performed in acute COVID-19 pneumonia: first report. Adv Respir Med. 2021;89(1):72-4. doi: 10.5603/ARM.a2021.0032
- De Gopegui Miguelena PR, Chamarro MP, Vega LMC. Afectación endotelial por Covid-19 en criobiopsia pulmonar. Archivos de Bronconeumología. 2020;57:65. doi: 10.1016/j.arbres.2020.06.010
- Doglioni C, Ravaglia C, Rossi G, et al. Acute Lung injury evolution in Covid-19. MedRxiv. 2020. doi: 10.1101/2020.08.09.20170910
- Barisione E, Grillo F, Ball L, et al. Fibrotic progression and radiologic correlation in matched lung samples from COVID-19 post-mortems. Virchows Arch. 2021;478(3):471-85. doi: 10.1007/s00428-020-02934-1
- Su Y, Yuan D, Chen DG, et al. Multiple early factors anticipate post-acute COVID-19 sequelae. Cell. 2022;185(5):881-95.e20. doi: 10.1016/j.cell.2022.01.014
- Bastard P, Gervais A, Le Voyer T, et al. Autoantibodies neutralizing type I IFNs are present in ~4% of uninfected individuals over 70 years old and account for ~20% of COVID-19 deaths. Sci Immunol. 2021;6(62):eabl4340. doi: 10.1126/sciimmunol.abl4340
- Wang C, Wang Z, Wang G, et al. COVID-19 in early 2021: current status and looking forward. Signal Transduct Target Ther. 2021;6(1):114. doi: 10.1038/s41392-021-00527-1
- Bone RC. Toward a theory regarding the pathogenesis of the systemic inflammatory response syndrome: what we do and do not know about cytokine regulation. Crit Care Med. 1996;24(1):163-72. doi: 10.1097/00003246-199601000-00026
- Chang S, Pierson E, Koh PW, et al. Mobility network models of COVID-19 explain inequities and inform reopening. Nature. 2021;589(7840):82-7. doi: 10.1038/s41586-020-2923-3
- Parasa S, Desai M, Thoguluva Chandrasekar V, et al. Prevalence of Gastrointestinal Symptoms and Fecal Viral Shedding in Patients With Coronavirus Disease 2019: A Systematic Review and Meta-analysis. JAMA Netw Open. 2020;3(6):e2011335. doi: 10.1001/jamanetworkopen.2020.11335
- Hotchkiss RS, Monneret G, Payen D. Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach. Lancet Infect Dis. 2013;13(3):260-8. doi: 10.1016/S1473-3099(13)70001-X
- Sugimoto MA, Sousa LP, Pinho V, et al. Resolution of Inflammation: What Controls Its Onset? Front Immunol. 2016;7:160. doi: 10.3389/fimmu.2016.00160
- Bozza FA, Salluh JI, Japiassu AM, et al. Cytokine profiles as markers of disease severity in sepsis: a multiplex analysis. Crit Care. 2007;11(2):R49. doi: 10.1186/cc5783
- Pretorius L, Kell DB, Pretorius E. Iron Dysregulation and Dormant Microbes as Causative Agents for Impaired Blood Rheology and Pathological Clotting in Alzheimer's Type Dementia. Front Neurosci. 2018;12:851. doi: 10.3389/fnins.2018.00851
- Fitridge R, Thompson M, eds. Mechanisms of Vascular Disease: A Reference Book for Vascular Specialists. Adelaide (AU): University of Adelaide Press, 2011.
- Hamers L, Kox M, Pickkers P. Sepsis-induced immunoparalysis: mechanisms, markers, and treatment options. Minerva Anestesiol. 2015;81(4):426-39.
- Walton AH, Muenzer JT, Rasche D, et al. Reactivation of multiple viruses in patients with sepsis. PLoS One. 2014;9(2):e98819. doi: 10.1371/journal.pone.0098819
- Xu K, Cai H, Shen Y, et al. Management of COVID-19: the Zhejiang experience. Zhejiang Da Xue Xue Bao Yi Xue Ban. 2020;49(2):147-57. doi: 10.3785/j.issn.1008-9292.2020.02.02
- Baek MS, Cha MJ, Kim MC, et al. Clinical and radiological findings of adult hospitalized patients with community-acquired pneumonia from SARS-CoV-2 and endemic human coronaviruses. PLoS One. 2021;16(1):e0245547. doi: 10.1371/journal.pone.0245547
- Di Felice G, Visci G, Teglia F, et al. Effect of cancer on outcome of COVID-19 patients: a systematic review and meta-analysis of studies of unvaccinated patients. Elife. 2022;11:e74634. doi: 10.7554/eLife.74634
- Wei J, Alfajaro MM, DeWeirdt PC, et al. Genome-wide CRISPR Screens Reveal Host Factors Critical for SARS-CoV-2 Infection. Cell. 2021;184(1):76-91.e13. doi: 10.1016/j.cell.2020.10.028
- Truong TT, Ryutov A, Pandey U, et al. Increased viral variants in children and young adults with impaired humoral immunity and persistent SARS-CoV-2 infection: A consecutive case series. EBioMedicine. 2021;67:103355. doi: 10.1016/j.ebiom.2021.103355
- Choi B, Choudhary MC, Regan J, et al. Persistence and Evolution of SARS-CoV-2 in an Immunocompromised Host. N Engl J Med. 2020;383(23):2291-3. doi: 10.1056/NEJMc2031364
- Obeid M, Suffiotti M, Pellaton C, et al. Humoral Responses Against Variants of Concern by COVID-19 mRNA Vaccines in Immunocompromised Patients. JAMA Oncol. 2022;8(5):e220446. doi: 10.1001/jamaoncol.2022.0446
- Sjöwall J, Azharuddin M, Frodlund M, et al. SARS-CoV-2 Antibody Isotypes in Systemic Lupus Erythematosus Patients Prior to Vaccination: Associations With Disease Activity, Antinuclear Antibodies, and Immunomodulatory Drugs During the First Year of the Pandemic. Front Immunol. 2021;12:724047. doi: 10.3389/fimmu.2021.724047
- Huang L, Li X, Gu X, et al. Health outcomes in people 2 years after surviving hospitalisation with COVID-19: a longitudinal cohort study. Lancet Respir Med. 2022;10(9):863-76. doi: 10.1016/S2213-2600(22)00126-6
- Moss P. The T cell immune response against SARS-CoV-2. Nat Immunol. 2022;23(2):186-93. doi: 10.1038/s41590-021-01122-w
- Mohanraj D, Bicknell K, Bhole M, et al. Antibody Responses to SARS-CoV-2 Infection-Comparative Determination of Seroprevalence in Two High-Throughput Assays versus a Sensitive Spike Protein ELISA. Vaccines (Basel). 2021;9(11):1310. doi: 10.3390/vaccines9111310
- Sherina N, Piralla A, Du L, et al. Persistence of SARS-CoV-2-specific B and T cell responses in convalescent COVID-19 patients 6-8 months after the infection. Med. 2021;2(3):281-95.e4. doi: 10.1016/j.medj.2021.02.001
- Jung JH, Rha MS, Sa M, et al. SARS-CoV-2-specific T cell memory is sustained in COVID-19 convalescent patients for 10 months with successful development of stem cell-like memory T cells. Nat Commun. 2021;12(1):4043. doi: 10.1038/s41467-021-24377-1
- Zuo J, Dowell AC, Pearce H, et al. Robust SARS-CoV-2-specific T cell immunity is maintained at 6 months following primary infection. Nat Immunol. 2021;22(5):620-6. doi: 10.1038/s41590-021-00902-8
- Izadi Z, Brenner EJ, Mahil SK, et al. Association Between Tumor Necrosis Factor Inhibitors and the Risk of Hospitalization or Death Among Patients With Immune-Mediated Inflammatory Disease and COVID-19. JAMA Netw Open. 2021;4(10):e2129639. doi: 10.1001/jamanetworkopen.2021.29639
- Ahmed H, Patel K, Greenwood DC, et al. Long-term clinical outcomes in survivors of severe acute respiratory syndrome and Middle East respiratory syndrome coronavirus outbreaks after hospitalisation or ICU admission: A systematic review and meta-analysis. J Rehabil Med. 2020;52(5):jrm00063. doi: 10.2340/16501977-2694
- Marvisi M, Ferrozzi F, Balzarini L, et al. First report on clinical and radiological features of COVID-19 pneumonitis in a Caucasian population: Factors predicting fibrotic evolution. Int J Infect Dis. 2020;99:485-8. doi: 10.1016/j.ijid.2020.08.054
- Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497-506. doi: 10.1016/S0140-6736(20)30183-5
- Ojo AS, Balogun SA, Williams OT, Ojo OS. Pulmonary Fibrosis in COVID-19 Survivors: Predictive Factors and Risk Reduction Strategies. Pulm Med. 2020;2020:6175964. doi: 10.1155/2020/6175964
- Gao YD, Ding M, Dong X, et al. Risk factors for severe and critically ill COVID-19 patients: A review. Allergy. 2021;76(2):428-55. doi: 10.1111/all.14657
- Hu ZJ, Xu J, Yin JM, et al. Lower Circulating Interferon-Gamma Is a Risk Factor for Lung Fibrosis in COVID-19 Patients. Front Immunol. 2020;11:585647. doi: 10.3389/fimmu.2020.585647