Endoscopic Features of Post-COVID-19 Cholangiopathy and Its Management Using ERCP

Abstract

Introduction: Despite growing awareness of post-coronavirus disease 2019 (COVID-19) cholangiopathy as one of the most serious long-term gastrointestinal consequences of COVID-19, the endoscopic features of this disease are still poorly characterized. This study aimed to more precisely define its endoscopic features and to outline the role of endoscopic retrograde cholangiopancreatography (ERCP) in the management of this entity.

Methods: In this observational study, 46 patients with confirmed post-COVID-19 cholangiopathy were included.

Results: Based on the endoscopic features observed in 141 ERCP procedures, post-COVID-19 cholangiopathy can be classified as a variant of secondary sclerosing cholangitis in critically ill patients. It appeared early in the course of intensive care treatment of patients with COVID-19 (cholestasis onset 4.5 days after intubation, median). This form of cholangiopathy was more destructive than stricturing in nature and caused irreversible damage to the bile ducts. A centripetal pattern of intrahepatic bile duct destruction, the phenomenon of vanishing bile ducts, the absence of extrahepatic involvement, and the presence of intraductal biliary casts (85% of patients) were typical cholangiographic features of post-COVID-19 cholangiopathy. This cholangiopathy was often complicated by small peribiliary liver abscesses with isolation of Enterococcus faecium and Candida spp. in bile culture. The prognosis was dismal, with a 1-year liver transplantation-free survival rate of 44%. In particular, patients with peribiliary liver abscesses or destruction of the central bile ducts tended to have a poor prognosis (n.s.). As shown by multivariate analysis, bilirubin levels (on intensive care unit day 25-36) negatively correlated with liver transplantation-free survival (hazard ratio 1.08, P < 0.001). Interventional endoscopy with cast removal had a positive effect on cholestasis parameters (gamma-glutamyl transpeptidase, alkaline phosphatase, and bilirubin); approximately 60% of all individual values decreased.

Discussion: Gastrointestinal endoscopy makes an important contribution to the management of post-COVID-19 cholangiopathy. ERCP is not only of great diagnostic and prognostic value but also has therapeutic value and therefore remains indispensable.

Graphical abstract

Figure 1.

Distribution pattern of the biliary lesions. (a) Hepatic duct type: ERCP in a 60-year-old man with post–COVID-19 cholangiopathy shows involvement of the left hepatic duct and the subsegmental and segmental branches; the patient did not survive. (b) Segmental type: ERCP in a 59-year-old woman with post–COVID-19 cholangiopathy shows that both hepatic ducts are intact but the peripheral, subsegmental, and segmental branches are affected; the patient did not survive. (c) Subsegmental type: ERCP in a 48-year-old man shows that the peripheral and subsegmental branches are affected, while the segmental branches and both hepatic bile ducts are preserved; the patient was alive at the end of follow-up. (d) Peripheral type: ERCP in a 53-year-old woman shows that the peripheral branches are affected, while the subsegmental and segmental branches and both hepatic bile ducts are preserved; the patient survived. COVID-19, coronavirus disease 2019; ERCP, endoscopic retrograde cholangiopancreatography.

Figure 2.

Anatomical distribution of biliary lesions in post–COVID-19 cholangiopathy. Frequency of each type of destruction in the overall cohort. (©2023/Christine Voigts/Charité.)

Figure 3.

Wall destruction characteristic of post–COVID-19 cholangiopathy. (a–d) Early stages: ERCP in 4 patients with post–COVID-19 cholangiopathy showed destruction of peripheral, subsegmental, and (predominantly) segmental branches of the biliary tree. (e–h) Late stages in 4 different patients: advanced loss of intrahepatic branches. COVID-19, coronavirus disease 2019; ERCP, endoscopic retrograde cholangiopancreatography.

Figure 4.

Biliary casts I. (a and c) Extracted casts of different shapes. (b) endoscopic retrograde cholangiopancreatography shows biliary casts as ribbon-like intraductal filling defects (arrow) (d) Radial endoscopic ultrasound (EUS) of the common bile duct shows biliary casts as hyperechogenic material (arrow). (c has been adapted from Leonhardt et al. doi: 10.1007/s00134-023-07257-8.)

Figure 5.

Biliary casts II. (a) Cast removal by endoscopic retrograde cholangiopancreatography. (b) Scanning electron microscopy of an extracted biliary cast from a 53-year-old woman with post–COVID-19 cholangiopathy (c) Scanning electron microscopy showed that the biliary casts contain collagen fibers. (d) Scanning electron microscopy showed casts overgrown by bacterial cocci.

Figure 6.

Liver abscesses in post–COVID-19 cholangiopathy. (a) CT of a 52-year-old man confirmed abscesses that were suspected in the ERCP 1 day before. (b) Same patient as in A: ERCP showed multiple small abscesses in the right hepatic lobe, the patient required LT. (c) Axial positron emission tomography-computed tomography showed multiple liver abscesses in a 60-year-old man with post–COVID-19 cholangiopathy. (d) Same patient as in C: frontal plane showed an abscess in the left liver lobe extending to the left ventricle. The patient did not survive. COVID-19, coronavirus disease 2019.

Figure 7.

Kaplan-Meier survival curve for overall survival. A total of 45 patients with post–COVID-19 cholangiopathy were included in the analysis. One patient of the cohort who was lost to follow-up was excluded.