PMC:7543426 / 6771-20816 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7543426","sourcedb":"PMC","sourceid":"7543426","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7543426","text":"RESULTS\n\nPatient Demographics and Clinical Characteristics\nTable 1 and Table 2 depict the demographic and clinical characteristics of 22 COVID-19 patients on whom postmortem examinations were performed. Of these, 18 had other medical comorbidities (designated group 1). Four patients were healthy prior to hospital admission and had no known medical comorbidities or any cause of immunosuppression (designated group 2).\nTable 1. Summary of Patient Demographics at Baseline\nCharacteristic Group 1 With Comorbidities Group 2 Without Comorbidities\nNumber of patients 18 4\nDemography\n Age, y, median ± SD (range) 76 ± 15.7 (27–92) 48.5 ± 13.07 (35–65)\n Men 12 (66.7) 3 (75)\n Women 6 (33.3) 1 (25)\nComorbidity\n Chronic obstructive pulmonary disease 6 (33.3) …\n Cardiac disease 8 (44.5) …\n Malignancy 5 (27.8) …\n Hypertension 4 (22.3) …\n Diabetes 4 (22.3) …\n Schizophrenia 1 (5.6) …\n Kidney disease 2 (11.2) …\nData are No. (%) except where indicated.\nTable 2. Demographics, Comorbidities, Duration of Hospital Stay, and Autopsy Cause of Death\nPatient Number Sex, M/F Age, y Onset of Symptoms, d Comorbidities Days in Hospital Before Death Postmortem Cause of Death\n1 M 81 Not known Hypertension Aortomyocardial sclerosis Ischemic heart disease Cardiomyopathy Aortic aneurysm 4 Cardiorespiratory failure\n2 F 82 Not known Diabetes Atrioventricular valve prothesis Atrial fibrillation COPD Malignancy Kidney disease 3 Cardiorespiratory failure\n3 M 92 7 COPD 1 Cardiorespiratory failure\n4 F 69 Not known Schizophrenia 28 Cardiorespiratory failure\n5 F 80 Not known Cardiovascular disease Senile dementia 38 Cardiorespiratory failure\n6 M 92 Not known Cardiovascular disease COPD 3 Cardiorespiratory failure\n7 F 64 4 Malignancy 2 Cardiorespiratory failure\n8 M 58 Not known Pulmonary artery thrombosis 4 Cardiorespiratory failure\n9 M 64 Not known Myelodysplasia 4 Cardiorespiratory failure\n10 M 82 3 Aortic aneurysm COPD 5 Cardiorespiratory failure\n11 M 76 Not known Malignancy 30 Cardiorespiratory failure\n12 M 60 6 Malignancy Hypertension Kidney disease Diabetes COPD Obesity 29 Cardiorespiratory failure\n13 F 70 Not known Cardiovascular disease Diabetes Psychiatric disorder 43 Cardiorespiratory failure\n14 M 76 Not known Malignancy COPD Hypertension Cardiovascular disease 33 Cardiorespiratory failure\n15 F 27 Not known HIV infection 6 Cardiorespiratory failure\n16 M 82 Not known Parkinson disease Hypertension Transient ischemic attack Prostate hypertrophy 14 Cardiorespiratory failure\n17 M 57 Not known Diabetes 1 Cardiorespiratory failure\n18 M 86 Not known Endocarditis caused by Staphylococcus aureus Prostate hypertrophy Aortic aneurysm Atrial fibrillation 1 Cardiorespiratory failure\n19 M 54 4 NONE 16 Cardiorespiratory failure\n20 M 35 5 NONE 7 Cardiorespiratory failure\n21 M 65 7 NONE 12 Cardiorespiratory failure\n22 F 43 Not known NONE 25 Cardiorespiratory failure\nAbbreviation: COPD, chronic obstructive pulmonary disease.\n\nAutopsy and Microscopic Examination\n\nLung Findings\n\nMacroscopic Findings.\nLungs from all patients were increased in volume, firm, edematous, and congested with diffuse pleural thickening and pleural effusion. Cut surface showed consolidation of lobes and red congested areas, with thickening of the interstitial septa and pulmonary edema (Figure 1A1). Subsegmental pulmonary embolism was seen in 5 cases.\nFigure 1. Pathological findings in lung. A1, Lungs showed an increase in volume and were firmer and heavier than normal. A2 and A3, Light microscopic analysis shows parenchymal multifocal damage with intraalveolar inflammation, fibrin, and hyaline membranes consistent with a diagnosis of diffuse alveolar damage. Both acute exudative inflammatory process and fibrous proliferative phase were found. A3 and A4, Hyperplasia of type II pneumocyte, characterized by amphophilic cytoplasm, large nuclei, and prominent nucleoli, are shown (arrows). B1, Alveolar duct fibrosis. B2, Fibrin thrombi in capillaries. B3, Vascular injury including vessel vasculitis and vascular edema. B4, Pleural fibrosis. Abbreviation: H\u0026E, haematoxylin and eosin. Scale bars: A2, 14 µm; A3–B3, 7 µm; B4, 21 µm.\n\nMicroscopic Findings.\nA range of common lung findings were seen on light microscopy. Parenchymal multifocal damage with intraalveolar exudative and proliferative inflammation (Figure 1A2), with fibrin, hyaline membranes (Figure 1A3) consistent with a diagnosis of diffuse alveolar damage (Table 3). Organizing pneumonia with fibrosis and type II pneumocyte hyperplasia, amphophilic cytoplasm, large nuclei, and prominent nucleoli, were indicative of cytopathic virus-induced changes (Figure 1A3 and 1A4). Fibroblastic foci consisting of loose organizing connective tissue reflective of alveolar duct fibrosis were seen (fibrotic phase) (Figure 1B1). Other findings included: pleural fibrosis (Figure 1B4), vascular injury with thrombi (Figure 1B2), and vasculitis (Figure 1B3). A main feature was the presence of numerous inflammatory cells consisting of granulocytes (CD15+) (Supplementary Figure 1A1 and 1A2), macrophages (CD68+) (Supplementary Figure 1A3 and 1A4), and T lymphocytes (CD3+) infiltrating into alveolar septa and clustering around capillary vessels (Supplementary 1B1). Immunohistochemistry showed the presence of both CD4+ and CD8+ T lymphocytes (Supplementary Figure 1B2 and 1B3). Of note, lymphocytes were CD20− indicating an absence of infiltrating B lymphocytes. Thrombi were present and immunohistochemistry showed the presence of platelet aggregates and megakaryocytes within thrombi (Supplementary Figure 1B4).\nTable 3. Histopathology Findings\nFindings Group 1, No. (%) (n = 18) Group 2, No. (%) (n = 4)\nLung\n Hyaline membranes 8 (44.4) 2 (50.0)\n Hyperplasia of type II pneumocyte 11 (61.2) 4 (100)\n Alveolar plug 8 (44.4) 4 (100)\n Alveolar fibrin deposit 9 (50.0) 3 (75.0)\n Hemorrhage 10 (55.6) 2 (50.0)\n Inflammatory cells 13 (72.3) 4 (100)\n Diffuse alveolar damage, fibrotic phase 12 (66.7) 1 (25.0)\n Microthrombi 14 (77.8) 2 (50.0)\n Vasculitis 8 (44.4) 4 (100)\n Multinucleated giant cells 4 (22.3) 2 (50.0)\nCardiac\n Myocarditis 9 (50.0) 3 (75.0)\n Vasculitis 5 (27.8) 3 (75.0)\n Inflammatory infiltrate 13 (72.3) 3 (75.0)\n Focal necrosis 6 (33.4) 2 (50.0)\n Pericarditis 9 (50.0) 4 (100)\n Vascular fibrosis 4 (22.3) 2 (50.0)\nHepatic\n Inflammatory infiltrate 8 (44.4) 3 (75.0)\n Congestion 8 (44.4) 2 (50.0)\n Steatosis 9 (50.0) 3 (75.0)\nRenal\n Inflammatory infiltrate 9 (50.0) 3 (75.0)\n Glomerulosclerosis 9 (50.0) 3 (75.0)\n Interstitial fibrosis 9 (50.0) 4 (100)\nSplenic\n Congested red pulp 15 (83.4) 4 (100)\n Lymphoid hypoplasia 11 (61.2) 4 (100)\nBone marrow\n Megakaryocytes hyperplasia 0 2 (50.0)\n Adipocytes 7 (38.9) 1 (25.0)\n\nImmunohistochemistry Findings.\nT-cell activation is modulated by dipeptidyl peptidase-4 (DPP4) [16] and thus the expression of CD26/DPP4 and CXCR3/CD183 was analyzed on lung tissues from group 2 patients (Figure 2). Numerous CD26+ cells were found in the alveolar septa (Figure 2A1–2A3) with intense staining seen in the type II pneumocytes (Figure 2A3). Positive cells entrapped with fibrin clots in the vascular lumen were also observed (Figure 2A4). CXCR3 immunostaining showed lymphocytes localized in inflammatory perivascular aggregates (Figure 2B1, 2B2, and 2B4) which spread into alveolar septa and alveolar spaces (Figure 2B2 and 2B3).\nFigure 2. Immunohistological characterization of lung tissue. A1–A4, CD26/dipeptidyl peptidase-4 expression in lung tissue. Numerous strongly positive CD26+ cells are seen in the alveolar septa. A3, Intense staining is seen in the type II pneumocytes (arrows). A4, Positive cells are also seen entrapped with fibrin in the vascular lumen. B1–B4, CXCR3/CD183 immunostaining shows intense staining of lymphocytes localized in the inflammatory perivascular aggregates and spread into alveolar septa and alveolar spaces. Scale bars: A1 and B1, 100 µm; A2, A3, and B4, 7 µm; A4, B2, and B3, 14 µm.\n\nElectron Microscopic Findings.\nSARS-CoV-2 particles were detected within type II pneumocytes, which showed degenerating features characterized by fine and uniformly dispersed chromatin. These pneumocytes displayed swollen mitochondrial profiles and dilated rough endoplasmic reticulum (Figure 3). Numerous virus-containing compartments (VCC) of different sizes and shapes were detected (Figure 3A, 3B, and 3D). Interestingly, spherules, very small vesicles containing single viral particles (Figure 3B and 3C), were also observed.\nFigure 3. SARS-CoV-2 detection in lung tissue by transmission electron microscopy. A, SARS-CoV-2 particles are visible in virus-containing compartments in type II pneumocytes (arrows). B–D, Numerous viral particles are enclosed in single-membrane vacuoles (arrow). Other, very small vesicles contain single viral particles (arrowheads). Scale bars: A, 1 µm; B–D, 200nm.\n\nHeart Findings\n\nMacroscopic Findings.\nThe hearts in all group 1 and 2 patients showed increased size and weight, hypertrophy, and dilation of the left and right atria and ventricles. The myocardium appeared pale and flabby, and endocardium showed punctuate petechial hemorrhages (Figure 4A1). Some patients in group 1 had pathological changes that were related to the patient’s age. These included myocardial ischemic or inflammatory changes, hypertensive changes of the left ventricular cavity, and valvular calcification of the mitral annulus and aortic valve (Figure 4A2).\nFigure 4. Histological changes in heart. A1, Hearts were increased in size and weight. The myocardium appeared pale and flabby. Endocardium showed punctuate petechial hemorrhages. A2, Age-related disease of the heart was represented by volume changes of the left ventricular cavity and exacerbated by systemic hypertension with valve changes including calcification of the mitral annulus and aortic valve. A3 and A4, Heart tissue shows myocytes hypertrophy, and variable degrees of interstitial and vascular fibrosis with mononuclear cells infiltrating adventitia. B1, Active myocarditis was characterized by mononuclear, predominantly lymphocytic infiltrate, associated with focal myocytes necrosis (B2). B3, Fibrinous, hemorrhagic areas with myofibers disarray were present. B4, Pericarditis with lymphocytic infiltration and increase in fibrous tissue was seen in all patients. Abbreviation: H\u0026E, haematoxylin and eosin. Scale bars: A3 and B4, 21 µm; A4–B2,7 µm; B3, 14 µm.\n\nMicroscopic Findings.\nMicroscopic changes seen were hypertrophy of myocytes and variable degrees of interstitial and vascular fibrosis (Figure 4A3 and 4A4). Mononuclear cells infiltrating adventitia was found predominantly in group 2 patients (Figure 4A4). Active myocarditis (Figure 4B1) characterized by mononuclear, predominantly lymphocytic, infiltrate, and was associated with focal myocytes necrosis (Figure 4B2), fibrinous, and hemorrhagic areas with myofibers disarray (Figure 4B3). Pericarditis (fibrinous or fibrous) was seen mainly in group 2 patients (Figure 4B4).\n\nLiver, Kidney, Spleen, and Bone Marrow Findings\n\nLiver.\nMacroscopic inspection of the liver of all patients showed parenchyma congestion. The main findings at histological level were sinusoidal congestion and extravasation of red blood cells into the space of Disse (Figure 5A1) and in a few cases this was associated with congestion of small veins and hepatocyte necrosis (Figure 5A2 and 5A3) and infiltration (Figure 5A4). Macrovacuolar and microvacuolar steatosis was seen mostly in group 2 patients (Figure 5A1, 5A2, and 5A4, and Table 3).\nFigure 5. Pathological findings in liver and kidney. A1, Liver tissue shows sinusoidal congestion and extravasation of red blood cells into the space of Disse. In some cases, small vein congestion (A2) and hepatic necrosis (A3) were reported. A4, Inflammatory infiltration was observed. A1, A2, and A4, Macrovacuolar and microvacuolar steatosis were observed in the majority of cases. B1, Kidney glomerular endothelial cells were swollen. B2, Fibrin deposit is visible underneath the Bowman capsule. B3, Tubulointerstitial inflammation and (B4) glomerular sclerosis were observed. Abbreviation: H\u0026E, haematoxylin and eosin. Scale bars: A1–A4, and B3, 50 µm; B1, B2, and B4, 14 µm\n\nKidney.\nThe kidneys of all patients generally had normal shape with reduced volume and size. Outer surfaces showed reddish depressions. Histological examination showed interstitial fibrosis, mainly in group 2 patients (Figure 5B1), with swollen glomerular endothelial cells. Fibrin deposits were visible underneath the Bowman capsule (Figure 5B2). Chronic tubular-interstitial inflammation (Figure 5B3) and glomerular sclerosis were observed (Figure 5B4) even in patients without a history of previous kidney disease (Table 3).\n\nSpleen.\nThe spleens of all patients had normal shape but reduced volume and size. The splenic white pulps of all 4 of the group 2 cases showed lymphoid hypoplasia with congested red pulp (Figure 6A1 and 6A2), and Table 3).\nFigure 6. Histology of spleen and bone marrow. A1 and A2, Lymphoid hypoplasia is visible in the splenic white pulp. B1 and B2, Bone marrows tissue shows replacement of red hematopoietic bone marrow with yellow adipocyte-rich marrow. Megakaryocyte hyperplasia is observed (arrows). Abbreviation: H\u0026E, haematoxylin and eosin. C1, Macrophages (CD68+) are present in bone marrow tissue. C2, CD68+ cells displaying features of hemophagocytosis (arrow). Scale bars: A1, A2, B2–C2, 7 µm; B1, 100 µm.\n\nBone Marrow.\nMicroscopic analysis of the bone marrows generally showed replacement of red hematopoietic bone marrow with yellow adipocyte-rich marrow in group 1 patients (Figure 6B1). Megakaryocytes hyperplasia (Figure 6B2) was seen in 2 patients of group 2 (Table 3). Numerous macrophages (CD68+) were seen and they displayed features of hemophagocytosis (Figure 6C1 and 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