Lung Histopathology in Coronavirus Disease 2019 as Compared With Severe Acute Respiratory Sydrome and H1N1 Influenza
2020; Elsevier BV; Volume: 159; Issue: 1 Linguagem: Inglês
10.1016/j.chest.2020.09.259
ISSN1931-3543
AutoresLida P. Hariri, Crystal M. North, Angela R. Shih, Rebecca A. Israel, Jason H. Maley, Julian A. Villalba, Vladimir Vinarsky, Jonah Rubin, Daniel Okin, Alyssa Sclafani, Jehan Alladina, Jason W. Griffith, Michael A. Gillette, Yuval Raz, C. Richards, Alexandra K. Wong, Amy Ly, Yin P. Hung, Raghu R. Chivukula, Camille R. Petri, Tiara F. Calhoun, Laura Brenner, Kathryn A. Hibbert, Benjamin D. Medoff, C. Corey Hardin, James R. Stone, Mari Mino‐Kenudson,
Tópico(s)Respiratory Support and Mechanisms
ResumoBackgroundPatients with severe coronavirus disease 2019 (COVID-19) have respiratory failure with hypoxemia and acute bilateral pulmonary infiltrates, consistent with ARDS. Respiratory failure in COVID-19 might represent a novel pathologic entity.Research QuestionHow does the lung histopathology described in COVID-19 compare with the lung histopathology described in SARS and H1N1 influenza?Study Design and MethodsWe conducted a systematic review to characterize the lung histopathologic features of COVID-19 and compare them against findings of other recent viral pandemics, H1N1 influenza and SARS. We systematically searched MEDLINE and PubMed for studies published up to June 24, 2020, using search terms for COVID-19, H1N1 influenza, and SARS with keywords for pathology, biopsy, and autopsy. Using PRISMA-Individual Participant Data guidelines, our systematic review analysis included 26 articles representing 171 COVID-19 patients; 20 articles representing 287 H1N1 patients; and eight articles representing 64 SARS patients.ResultsIn COVID-19, acute-phase diffuse alveolar damage (DAD) was reported in 88% of patients, which was similar to the proportion of cases with DAD in both H1N1 (90%) and SARS (98%). Pulmonary microthrombi were reported in 57% of COVID-19 and 58% of SARS patients, as compared with 24% of H1N1 influenza patients.InterpretationDAD, the histologic correlate of ARDS, is the predominant histopathologic pattern identified in lung pathology from patients with COVID-19, H1N1 influenza, and SARS. Microthrombi were reported more frequently in both patients with COVID-19 and SARS as compared with H1N1 influenza. Future work is needed to validate this histopathologic finding and, if confirmed, elucidate the mechanistic underpinnings and characterize any associations with clinically important outcomes. Patients with severe coronavirus disease 2019 (COVID-19) have respiratory failure with hypoxemia and acute bilateral pulmonary infiltrates, consistent with ARDS. Respiratory failure in COVID-19 might represent a novel pathologic entity. How does the lung histopathology described in COVID-19 compare with the lung histopathology described in SARS and H1N1 influenza? We conducted a systematic review to characterize the lung histopathologic features of COVID-19 and compare them against findings of other recent viral pandemics, H1N1 influenza and SARS. We systematically searched MEDLINE and PubMed for studies published up to June 24, 2020, using search terms for COVID-19, H1N1 influenza, and SARS with keywords for pathology, biopsy, and autopsy. Using PRISMA-Individual Participant Data guidelines, our systematic review analysis included 26 articles representing 171 COVID-19 patients; 20 articles representing 287 H1N1 patients; and eight articles representing 64 SARS patients. In COVID-19, acute-phase diffuse alveolar damage (DAD) was reported in 88% of patients, which was similar to the proportion of cases with DAD in both H1N1 (90%) and SARS (98%). Pulmonary microthrombi were reported in 57% of COVID-19 and 58% of SARS patients, as compared with 24% of H1N1 influenza patients. DAD, the histologic correlate of ARDS, is the predominant histopathologic pattern identified in lung pathology from patients with COVID-19, H1N1 influenza, and SARS. Microthrombi were reported more frequently in both patients with COVID-19 and SARS as compared with H1N1 influenza. Future work is needed to validate this histopathologic finding and, if confirmed, elucidate the mechanistic underpinnings and characterize any associations with clinically important outcomes. The Coronavirus Disease 2019 (COVID-19) pandemic, caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has swept throughout the world and captured our undivided attention.1Xu Z. Shi L. Wang Y. et al.Pathological findings of COVID-19 associated with acute respiratory distress syndrome.Lancet Respir Med. 2020; 8: 420-422Abstract Full Text Full Text PDF PubMed Scopus (6276) Google Scholar,2Wu F. Zhao S. Yu B. et al.A new coronavirus associated with human respiratory disease in China.Nature. 2020; 579: 265-269Crossref PubMed Scopus (7453) Google Scholar The novelty of the virus and massive burden of respiratory failure associated with it have led to urgent questions about its disease pathogenesis and pulmonary pathology. Both the scientific literature and media suggest that respiratory failure in COVID-19 represents a novel entity.3Gattinoni L. Chiumello D. Caironi P. et al.COVID-19 pneumonia: different respiratory treatments for different phenotypes?.Intensive Care Med. 2020; 46: 1099-1102Crossref PubMed Scopus (1221) Google Scholar,4Gattinoni L. Coppola S. Cressoni M. Busana M. Rossi S. Chiumello D. Covid-19 does not lead to a "typical" acute respiratory distress syndrome.Am J Respir Crit Care Med. 2020; 201: 1299-1300Crossref PubMed Scopus (954) Google Scholar However, clinical case series of patients with COVID-19 describe respiratory failure with moderate to severe hypoxemia and acute bilateral pulmonary infiltrates consistent with prior reports of ARDS, the most severe form of acute lung injury (ALI).1Xu Z. Shi L. Wang Y. et al.Pathological findings of COVID-19 associated with acute respiratory distress syndrome.Lancet Respir Med. 2020; 8: 420-422Abstract Full Text Full Text PDF PubMed Scopus (6276) Google Scholar,2Wu F. Zhao S. Yu B. et al.A new coronavirus associated with human respiratory disease in China.Nature. 2020; 579: 265-269Crossref PubMed Scopus (7453) Google Scholar,5Ziehr D.R. Alladina J. Petri C.R. et al.Respiratory pathophysiology of mechanically ventilated patients with COVID-19: a cohort study.Am J Respir Crit Care Med. 2020; 201: 1560-1564Crossref PubMed Scopus (323) Google Scholar Histopathologically, ALI is associated with a variety of manifestations that include diffuse alveolar damage (DAD), acute fibrinous and organizing pneumonia (AFOP), and organizing pneumonia (OP).6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar DAD lies on the severe end of the ALI spectrum and is the histopathologic pattern typically associated with clinical ARDS. DAD is caused by "endothelial and alveolar lining cell injury which leads to fluid and cellular exudation," culminating in physical disruption of the blood-air barrier.7Katzenstein A.L. Bloor C.M. Leibow A.A. Diffuse alveolar damage: the role of oxygen, shock, and related factors. A review.Am J Pathol. 1976; 85: 209-228PubMed Google Scholar DAD is divided into three histopathological phases that generally correlate with the time from pulmonary injury: acute (exudative) phase, subacute (organizing) phase, and chronic (fibrotic) phase.6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar, 7Katzenstein A.L. Bloor C.M. Leibow A.A. Diffuse alveolar damage: the role of oxygen, shock, and related factors. A review.Am J Pathol. 1976; 85: 209-228PubMed Google Scholar, 8Marshall R.P. Bellingan G. Webb S. et al.Fibroproliferation occurs early in the acute respiratory distress syndrome and impacts on outcome.Am J Respir Crit Care Med. 2000; 162: 1783-1788Crossref PubMed Scopus (227) Google Scholar The acute phase of DAD (Fig 1A) occurs within 1 week of the initial injury and is characterized by intra-alveolar hyaline membranes, edema, and alveolar wall thickening without significant inflammation, unless it arises in conjunction with acute pneumonia.6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar,7Katzenstein A.L. Bloor C.M. Leibow A.A. Diffuse alveolar damage: the role of oxygen, shock, and related factors. A review.Am J Pathol. 1976; 85: 209-228PubMed Google Scholar,9Leslie K.O. My approach to interstitial lung disease using clinical, radiological and histopathological patterns.J Clin Pathol. 2009; 62: 387-401Crossref PubMed Scopus (69) Google Scholar Vascular thrombosis and microthrombosis are frequently observed in DAD, even in the absence of a systemic hypercoagulable state, and they are thought to result from local inflammation.6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar,7Katzenstein A.L. Bloor C.M. Leibow A.A. Diffuse alveolar damage: the role of oxygen, shock, and related factors. A review.Am J Pathol. 1976; 85: 209-228PubMed Google Scholar,9Leslie K.O. My approach to interstitial lung disease using clinical, radiological and histopathological patterns.J Clin Pathol. 2009; 62: 387-401Crossref PubMed Scopus (69) Google Scholar,10Hariri L. Hardin C.C. Covid-19, angiogenesis, and ARDS endotypes.N Engl J Med. 2020; 383: 182-183Crossref PubMed Scopus (61) Google Scholar Angiographic studies also have confirmed that thrombosis occurs early in ARDS of diverse origins.11Greene R. Lind S. Jantsch H. et al.Pulmonary vascular obstruction in severe ARDS: angiographic alterations after i.v. fibrinolytic therapy.Am J Roentgenol. 1987; 148: 501-508Crossref PubMed Scopus (53) Google Scholar The subacute phase (Fig 1B) of DAD occurs approximately 1 week after the initial pulmonary injury and is characterized by microscopic organization of the fibrin followed by fibroblast migration and secretion of young "loose" collagen.6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar,7Katzenstein A.L. Bloor C.M. Leibow A.A. Diffuse alveolar damage: the role of oxygen, shock, and related factors. A review.Am J Pathol. 1976; 85: 209-228PubMed Google Scholar,9Leslie K.O. My approach to interstitial lung disease using clinical, radiological and histopathological patterns.J Clin Pathol. 2009; 62: 387-401Crossref PubMed Scopus (69) Google Scholar Hyaline membranes become slowly incorporated into organizing fibrotic tissue, which begins to appear in airspaces, alveolar ducts, and alveolar walls.6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar,7Katzenstein A.L. Bloor C.M. Leibow A.A. Diffuse alveolar damage: the role of oxygen, shock, and related factors. A review.Am J Pathol. 1976; 85: 209-228PubMed Google Scholar,9Leslie K.O. My approach to interstitial lung disease using clinical, radiological and histopathological patterns.J Clin Pathol. 2009; 62: 387-401Crossref PubMed Scopus (69) Google Scholar Reactive atypical changes in type II pneumocytes and squamous metaplasia may be present.6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar,7Katzenstein A.L. Bloor C.M. Leibow A.A. Diffuse alveolar damage: the role of oxygen, shock, and related factors. A review.Am J Pathol. 1976; 85: 209-228PubMed Google Scholar,9Leslie K.O. My approach to interstitial lung disease using clinical, radiological and histopathological patterns.J Clin Pathol. 2009; 62: 387-401Crossref PubMed Scopus (69) Google Scholar Some cases of DAD will ultimately resolve, whereas others evolve into a chronic fibrotic phase (weeks to months after the initial injury) with progressive architectural remodeling and interstitial fibrosis.6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar,7Katzenstein A.L. Bloor C.M. Leibow A.A. Diffuse alveolar damage: the role of oxygen, shock, and related factors. A review.Am J Pathol. 1976; 85: 209-228PubMed Google Scholar,9Leslie K.O. My approach to interstitial lung disease using clinical, radiological and histopathological patterns.J Clin Pathol. 2009; 62: 387-401Crossref PubMed Scopus (69) Google Scholar In the extreme, these changes may resemble usual interstitial pneumonitis, the histopathological correlate of idiopathic pulmonary fibrosis.6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar,7Katzenstein A.L. Bloor C.M. Leibow A.A. Diffuse alveolar damage: the role of oxygen, shock, and related factors. A review.Am J Pathol. 1976; 85: 209-228PubMed Google Scholar,9Leslie K.O. My approach to interstitial lung disease using clinical, radiological and histopathological patterns.J Clin Pathol. 2009; 62: 387-401Crossref PubMed Scopus (69) Google Scholar AFOP is characterized by formation of "fibrin balls" within the alveolar spaces, with organization resulting from fibroblast migration and secretion of young collagen within fibrin aggregates (Fig 1C).6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar,9Leslie K.O. My approach to interstitial lung disease using clinical, radiological and histopathological patterns.J Clin Pathol. 2009; 62: 387-401Crossref PubMed Scopus (69) Google Scholar,12Beasley M.B. Franks T.J. Galvin J.R. Gochuico B. Travis W.D. Acute fibrinous and organizing pneumonia: a histological pattern of lung injury and possible variant of diffuse alveolar damage.Arch Pathol Lab Med. 2002; 126: 1064-1070Crossref PubMed Google Scholar That DAD can have regions with AFOP features is well established. Therefore, the presence of hyaline membranes signifies a diagnosis of DAD, even if AFOP features are also present.6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar,9Leslie K.O. My approach to interstitial lung disease using clinical, radiological and histopathological patterns.J Clin Pathol. 2009; 62: 387-401Crossref PubMed Scopus (69) Google Scholar,12Beasley M.B. Franks T.J. Galvin J.R. Gochuico B. Travis W.D. Acute fibrinous and organizing pneumonia: a histological pattern of lung injury and possible variant of diffuse alveolar damage.Arch Pathol Lab Med. 2002; 126: 1064-1070Crossref PubMed Google Scholar OP can be seen in isolation or in combination with DAD or AFOP and is characterized by intraluminal tufts of plump fibroblasts and young/immature collagen tissue within alveolar ducts and distal airspaces (Fig 1D).6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar,9Leslie K.O. My approach to interstitial lung disease using clinical, radiological and histopathological patterns.J Clin Pathol. 2009; 62: 387-401Crossref PubMed Scopus (69) Google Scholar,12Beasley M.B. Franks T.J. Galvin J.R. Gochuico B. Travis W.D. Acute fibrinous and organizing pneumonia: a histological pattern of lung injury and possible variant of diffuse alveolar damage.Arch Pathol Lab Med. 2002; 126: 1064-1070Crossref PubMed Google Scholar DAD is considered to be the traditional histopathologic correlate of ARDS.6Beasley M.B. The pathologist's approach to acute lung injury.Arch Pathol Lab Med. 2010; 134: 719-727Crossref PubMed Google Scholar,7Katzenstein A.L. Bloor C.M. Leibow A.A. Diffuse alveolar damage: the role of oxygen, shock, and related factors. A review.Am J Pathol. 1976; 85: 209-228PubMed Google Scholar However, in a large study of 356 patients conducted by Thille et al,13Thille A.W. Esteban A. Fernandez-Segoviano P. et al.Comparison of the Berlin definition for acute respiratory distress syndrome with autopsy.Am J Respir Crit Care Med. 2013; 187: 761-767Crossref PubMed Scopus (300) Google Scholar fewer than half of patients with clinical ARDS, as defined by the Berlin criteria, had DAD on autopsy histopathology.13Thille A.W. Esteban A. Fernandez-Segoviano P. et al.Comparison of the Berlin definition for acute respiratory distress syndrome with autopsy.Am J Respir Crit Care Med. 2013; 187: 761-767Crossref PubMed Scopus (300) Google Scholar A published systematic review by Polak and colleagues14Polak S.B. Van Gool I.C. Cohen D. von der Thusen J.H. van Paassen J. A systematic review of pathological findings in COVID-19: a pathophysiological timeline and possible mechanisms of disease progression.Mod Pathol. 2020; 33: 2128-2138Crossref PubMed Scopus (317) Google Scholar described histologic patterns consistent with ARDS in lung tissue samples of patients with COVID-19, but whether the patterns of lung injury are unique to COVID-19 as compared with other viral causes of ARDS remains unknown.14Polak S.B. Van Gool I.C. Cohen D. von der Thusen J.H. van Paassen J. A systematic review of pathological findings in COVID-19: a pathophysiological timeline and possible mechanisms of disease progression.Mod Pathol. 2020; 33: 2128-2138Crossref PubMed Scopus (317) Google Scholar To address this gap in knowledge, we conducted a systematic review of the published literature on COVID-19 lung histopathology from a total of 171 described patients. To provide context for the histopathologic findings in COVID-19 as compared with other recent viral pandemics, we conducted additional systematic reviews of the published literature of lung histopathology reported in 287 patients infected with the 2009 influenza (H1N1) virus and 64 patients infected with SARS-CoV associated with the 2003 SARS outbreak. We conducted several literature natural language searches on MEDLINE, MedRxiv, arXiv, and PubMed, using multiple logical search terms as appropriate and in accordance with the PRISMA (Preferred Reporting Items for a Systematic Review and Meta-analysis) guidelines.15Moher D. Shamseer L. Clarke M. et al.Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement.Syst Rev. 2015; 4: 1Crossref PubMed Scopus (14965) Google Scholar We identified studies of COVID-19 lung histopathology through MEDLINE database searches for "(COVID-19 OR SARS-CoV-2) AND (Pathology OR Autopsy OR Biopsy)." Inclusion criteria for the COVID-19 systematic review included (1) confirmation of SARS-CoV-2 infection by real-time reverse-transcriptase polymerase chain reaction (RT-PCR) assay; (2) clinical suspicion of COVID-19 as the primary cause of death; and (3) sufficient histologic description of each reported case within the study. Preprint studies were not included in our analysis because of the lack of adequate peer review at the time of publication. We identified studies of 2009 H1N1 influenza lung histopathology through a PubMed search for "H1N1 AND (Pathology OR Autopsy OR Biopsy)." Inclusion criteria for the H1N1 influenza systematic review included (1) confirmation of H1N1 influenza infection by RT-PCR; (2) clinical suspicion of H1N1 infection as the primary cause of death, and (3) sufficient histologic description of each reported case within the study. We identified studies of 2003 SARS lung histopathology through a PubMed search for "SARS AND (Pathology OR Autopsy OR Biopsy)." Inclusion criteria for the SARS systematic review included: (1) fulfillment of the World Health Organization clinical criteria for SARS, including radiologic evidence of infiltrates consistent with pneumonia, fever > 38°C, and a history of chills, cough, malaise, or known exposure; (2) clinical suspicion of SARS-CoV infection as the primary cause of death; and (3) sufficient histologic description of each reported case. Data were extracted by two pathologists (L. H., A. S.) into a Microsoft Excel spreadsheet (2016 Version 15.28). Studies were separated into the following disease categories: COVID-19, 2009 H1N1 influenza, and SARS. The presence of key histologic features were identified and summarized in all studies, including DAD, AFOP, organizing fibrosis, end-stage fibrosis, superimposed neutrophilic pneumonia, microthrombi, and pulmonary thrombi. Categorical variables were expressed numerically (%). Using our search strategy, we identified 1,791 potentially relevant COVID-19 studies. Of these, 1,742 studies were excluded as not relevant (animal studies or studies without histopathology). Because of the global nature of the early literature, we included foreign language and non-pulmonary-specific studies for further review. We screened 49 studies by title and abstract, excluding an additional two studies as duplicates and one study as a preprint, and completed an in-depth review of the remaining 46 full-length articles (using online language translators for non-English articles as appropriate). A total of 26 articles representing 171 patients met the inclusion criteria and were included in this systematic review (Fig 2).1Xu Z. Shi L. Wang Y. et al.Pathological findings of COVID-19 associated with acute respiratory distress syndrome.Lancet Respir Med. 2020; 8: 420-422Abstract Full Text Full Text PDF PubMed Scopus (6276) Google Scholar,16Ackermann M. Verleden S.E. 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Kuehnel M. et al.Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in Covid-19.N Engl J Med. 2020; 383: 120-128Crossref PubMed Scopus (3783) Google Scholar,20Buja L.M. Wolf D.A. Zhao B. et al.The emerging spectrum of cardiopulmonary pathology of the coronavirus disease 2019 (COVID-19): report of 3 autopsies from Houston, Texas, and review of autopsy findings from other United States cities.Cardiovasc Pathol. 2020; 48: 107233Crossref PubMed Scopus (290) Google Scholar, 21Carsana L. Sonzogni A. Nasr A. et al.Pulmonary post-mortem findings in a series of COVID-19 cases from northern Italy: a two-centre descriptive study.Lancet Infect Dis. 2020; 20: 1135-1140Abstract Full Text Full Text PDF PubMed Scopus (883) Google Scholar, 22Copin M.-C. Parmentier E. Duburcq T. Poissy J. Mathieu D. Time to consider histologic pattern of lung injury to treat critically ill patients with COVID-19 infection.Intensive Care Med. 2020; 46: 1124-1126Crossref PubMed Scopus (197) Google Scholar,24Fox S.E. Akmatbekov A. Harbert J.L. Li G. Quincy Brown J. Vander Heide R.S. Pulmonary and cardiac pathology in African American patients with COVID-19: an autopsy series from New Orleans.Lancet Respir Med. 2020; 8: 681-686Abstract Full Text Full Text PDF PubMed Scopus (892) Google Scholar,26Konopka K.E. Nguyen T. Jentzen J.M. et al.Diffuse alveolar damage (DAD) from coronavirus disease 2019 infection is morphologically indistinguishable from other causes of DAD.Histopathology. 2020; ([Published online ahead of print June 15, 2020])https://doi.org/10.1111/his.14180Crossref PubMed Scopus (128) Google Scholar, 27Lax S.F. Skok K. Zechner P. et al.Pulmonary arterial thrombosis in COVID-19 with fatal outcome: results from a prospective, single-center, clinicopathologic case series.Ann Intern Med. 2020; ([Published online ahead of print May 14, 2020])https://doi.org/10.7326/M20-2566Crossref PubMed Scopus (571) Google Scholar, 28Magro C. Mulvey J.J. Berlin D. et al.Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: a report of five cases.Transl Res. 2020; 220: 1-13Abstract Full Text Full Text PDF PubMed Scopus (1613) Google Scholar, 29Martines R.B. Ritter J.M. Matkovic E. et al.Pathology and pathogenesis of SARS-CoV-2 associated with fatal coronavirus disease, United States.Emerg Infect Dis. 2020; 26: 2005-2015Crossref PubMed Scopus (266) Google Scholar, 30Menter T. Haslbauer J.D. Nienhold R. 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; 77: 198-209Crossref PubMed Scopus (878) Google Scholar, 31Nunes Duarte-Neto A. de Almeida Monteiro R.A. da Silva L.F.F. et al.Pulmonary and systemic involvement of COVID-19 assessed by ultrasound-guided minimally invasive autopsy.Histopathology. 2020; ([Published online ahead of print May 22, 2020])https://doi.org/10.1111/his.14160Crossref PubMed Scopus (240) Google Scholar, 32Schaller T
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