Pulmonary and cardiac pathology in African American patients with COVID-19: an autopsy series from New Orleans

Abstract

Background: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) spread rapidly across the USA, causing extensive morbidity and mortality, particularly in the African American community. Autopsy can considerably contribute to our understanding of many disease processes and could provide crucial information to guide management of patients with coronavirus disease 2019 (COVID-19). We report on the relevant cardiopulmonary findings in, to our knowledge, the first autopsy series of ten African American decedents, with the cause of death attributed to COVID-19.

Methods: Autopsies were performed on ten African American decedents aged 44-78 years with cause of death attributed to COVID-19, reflective of the dominant demographic of deaths following COVID-19 diagnosis in New Orleans. Autopsies were done with consent of the decedents' next of kin. Pulmonary and cardiac features were examined, with relevant immunostains to characterise the inflammatory response, and RNA labelling and electron microscopy on representative sections.

Findings: Important findings include the presence of thrombosis and microangiopathy in the small vessels and capillaries of the lungs, with associated haemorrhage, that significantly contributed to death. Features of diffuse alveolar damage, including hyaline membranes, were present, even in patients who had not been ventilated. Cardiac findings included individual cell necrosis without lymphocytic myocarditis. There was no evidence of secondary pulmonary infection by microorganisms.

Interpretation: We identify key pathological states, including thrombotic and microangiopathic pathology in the lungs, that contributed to death in patients with severe COVID-19 and decompensation in this demographic. Management of these patients should include treatment to target these pathological mechanisms.

Funding: None.

Figure 1

Gross findings of the lungs and heart (A) Lungs with bilateral pulmonary oedema and patches of dark haemorrhage. (B) Cut sections of lung showing thrombi present within peripheral small vessels (green arrows) (C) A heart showing extreme right ventricular dilatation, with straightening of the interventricular septum.

Figure 2

Pulmonary diffuse alveolar damage All patients had extensive diffuse alveolar damage. (A) Green arrows indicate early hyaline membranes in a patient with 1 week of symptomatic illness and no mechanical ventilation (H&E stain). (B) Green arrows indicate extensive hyaline membranes and fibrinous exudate in a patient with 9 days of symptomatic illness, including 6 days of ventilation (H&E stain). (C) Green arrow indicates dense hyaline membranes, with organising fibrosis (green arrowhead), and fibrin thrombi present in small vessels (blue arrows), with a pauci-immune and oedematous background in a patient after 32 days of illness, including 25 days on ventilatory support. Extensive haemorrhage was also present (H&E stain). (D) Bronchial respiratory epithelium shown with cilia present, and absence of squamous metaplasia in a patient receiving ventilatory support for 6 days. H&E=haematoxylin and eosin.

Figure 3

Pulmonary thrombi and microangiopathy (A) Thrombus in a small pulmonary artery (green arrow), with small thrombus seen in adjacent pulmonary venule (green arrowhead), with H&E present on the left, and CD61 immunostain highlighting platelets within the thrombi on the right. (B) Many megakaryocytes were present within the small vessels and alveolar capillaries (green arrow). (C) CD61 immunostain highlighting additional fibrin and platelet thrombus shown in a small vessel, with megakaryocyte stained below (green arrowhead). Von Willebrand Factor immunostain additionally highlighted these vessels (appendix p 8). (D) Small, perivascular aggregates of lymphocytes. Also present were small lymphocytic aggregates surrounding airways, which were positive for CD4 immunostain, with only scattered CD8 positive cells present (appendix p 7).

Figure 4

SARS-CoV-2 cytopathic effects (A) Several enlarged pneumocytes within a damaged alveolus, having enlarged nuclei, prominent nucleoli, and cytologic atypia (H&E stain). (B) Relative distribution of DNA (red) versus RNA (green) in tissue sections via DRAQ5 and SYTO RNASelect fluorescent staining (appendix p 1 for staining details). Pneumocytes with increased RNA in alveolar spaces show aggregation; enlarged, atypical morphology shown by DNA stain; and abundant RNA present within the cytoplasm (green arrows). (C) Entrapment of immune cells, including degenerated neutrophils, within fibrin, and strands of extracellular material with weak DNA staining. (D) Control lung tissue obtained at autopsy for non-pulmonary cause of death before the coronavirus disease 2019 pandemic. (E) Electron microscopy of the lung, showing particles suggestive of viral infection (examples highlighted by blue arrows. H&E=haematoxylin and eosin.

Figure 5

Cardiac microscopic findings A) patient 2, i: Cardiac myocytes, ii: CD4 immunostain, iii: CD8 immunostain. B) patient 3, i: Cardiac myocytes, ii: CD31 immunostain, iii: CD4 immunostain. Cardiac myocytes showing focal, atypical myocyte degeneration (green arrows), H&E stain (sample images from patients aged 44 and 63 years receiving azithromycin but not hydroxychloroquine). Scant lymphocytes were present within the interstitial and endothelial spaces, with slightly more CD4⁺ than CD8⁺ cells on visual inspection of immunostains. A CD31 immunostain highlighted endothelial cells, with focal prominence (green arrow) that appeared non-specific. CD4⁺ lymphocytes were occasionally seen in a non-specific pattern within the coronary artery intima. H&E=haematoxylin and eosin.