Retrospective Cohort Study
Copyright ©The Author(s) 2020. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Aug 7, 2020; 26(29): 4302-4315
Published online Aug 7, 2020. doi: 10.3748/wjg.v26.i29.4302
Evaluation of intrahepatic manifestation and distant extrahepatic disease in alveolar echinococcosis
Tilmann Graeter, Hai-Hua Bao, Rong Shi, Wen-Ya Liu, Wei-Xia Li, Yi Jiang, Julian Schmidberger, Eleonore Brumpt, Eric Delabrousse, Wolfgang Kratzer, the XUUB Consortium
Tilmann Graeter, Rong Shi, Department of Diagnostic and Interventional Radiology, University Hospital Ulm, Ulm 89081, Germany
Hai-Hua Bao, Wei-Xia Li, Qinghai University, Qinghai University First Affiliated Hospital, Xining 810001, Qinghai Province, China
Wen-Ya Liu, Yi Jiang, Xinjiang Medical University, First Affiliated Hospital, WHO Collaborating Centre on Prevention and Care Management of Echinococcosis, Urumqi 830054, Xinjiang Uyghur Autonomous Region, China
Julian Schmidberger, Wolfgang Kratzer, Department of Internal Medicine I, University Hospital Ulm, Ulm 89081, Germany
Eleonore Brumpt, Eric Delabrousse, WHO Collaborating Centre on Prevention and Treatment of Human Echinococcosis/National French Reference Centre for Echinococcosis, University Bourgogne Franche-Comté and Besançon University Hospital, Besançon 25030, France
Author contributions: The plan for this manuscript was developed during a personal XUUB meeting of the authors; the data were evaluated by the authors at a meeting in Besançon; all authors were involved in the interpretation of the results; Graeter T and Bao HH contributed equally to this work; Graeter T, Bao HH, Kratzer W, Delabrousse E and Liu WY prepared the first draft; the statistical analysis was performed by Schmidberger J, Brumpt E, Shi R, Li WX and Jiang Y; all partners read, amended, and approved the final version of the manuscript.
Supported by a German Research Foundation funded project called “ Establishment of a national database for alveolar echinococcosis” , No. KA 4356/3-1;“Implementation of interfaces for the standardization of national database systems for alveolar echinococcosis and its transformation processes” , No. KR 5204/1-2; Multiple imaging study of the Hepatic Alveolar Echinococcosis after albendazole treatment, the Qinghai Science and Technology Department, No. 2017-SF-158; and the Müller Holding Ltd. and Co. KG Ulm.
Institutional review board statement: The study was approved by the local ethics committee and conducted in accordance with the Declaration of Helsinki (ref. No. 409/15). Because of its retrospective design and pseudonymized evaluation of imaging, no ethics approval was necessary for France and China. All data were analyzed anonymously.
Informed consent statement: Because of the retrospective and anonymous character of this study the need for informed consent was waived by the institutional review board.
Conflict-of-interest statement: The authors declare that they have no competing interests.
Data sharing statement: The datasets used and analysed during the current study are available from the corresponding author on reasonable request.
STROBE statement: The authors have read the STROBE Statement-checklist of items, and the manuscript was prepared and revised according to the STROBE Statement-checklist of items.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See:
Corresponding author: Wolfgang Kratzer, MD, Professor, Department of Internal Medicine I, University Hospital Ulm, Albert-Einstein-Allee 23, Ulm 89081, Germany.
Received: April 3, 2020
Peer-review started: April 3, 2020
First decision: May 26, 2020
Revised: June 9, 2020
Accepted: July 23, 2020
Article in press: July 23, 2020
Published online: August 7, 2020

The main endemic areas of alveolar echinococcosis (AE) are in Central Europe and Western China. Both the infiltration of intrahepatic vascular and bile duct structures as well as extrahepatic disease can lead to further complications and may increase morbidity in patients with AE.


To evaluate vascular/biliary involvement in hepatic AE and its distant extrahepatic disease manifestations in an international collective was the aim.


Consecutively, five experienced examiners evaluated contrast-enhanced abdominal computed tomography (CT) scans for 200 patients with hepatic AE of each of four locations (n = 50) in Germany, France and China. Therefore, we retrospectively included the 50 most recent abdominal contrast-enhanced CT examinations at each center, performed because of hepatic AE from September 21, 2007 to March 21, 2018. AE liver lesions were classified according to the echinococcosis multilocularis Ulm classification for CT (EMUC-CT). Distant extrahepatic manifestations were documented either by whole body positron emission tomography–CT or with the addition of thoracic CT and cranial magnetic resonance imaging. Vascular/biliary involvement of the hepatic disease as well as the presence of distant extrahepatic manifestations were correlated with the EMUC-CT types of liver lesion. Statistical analysis was performed using SAS Version 9.4 (SAS Institute Inc., Cary, NC, United States).


Distant extrahepatic AE manifestations were significantly more frequent in China than in Europe (P = 0.0091). A significant relationship was found between the presence of distant extrahepatic disease and AE liver lesion size (P = 0.0075). Vascular/biliary structures were involved by the liver lesions significantly more frequently in China than in Europe (P < 0.0001), and vascular/biliary involvement depended on lesion size. Different morphological types of AE liver lesions led to varying frequencies of vascular/biliary involvement and were associated with different frequencies of distant extrahepatic manifestations: Vascular/biliary involvement as a function of lesions primary morphology ranged from 5.88% of type IV liver lesions to 100% among type III lesions. Type IV differed significantly in these associations from types I, II, and III (P < 0.0001). With respect to extrahepatic disease, the primary morphology types IV and V of liver lesions were not associated with any case of distant extrahepatic disease. In contrast, distant extrahepatic manifestations in types I–III were found to varying degrees, with a maximum of 22% for type III.


Different CT morphological patterns of hepatic AE lesions influence vascular/biliary involvement and the occurrence of distant extrahepatic manifestations. There are intercontinental differences regarding the characteristics of AE manifestation.

Keywords: Alveolar echinococcosis, Echinococcus multilocularis, Echinococcus multilocularis Ulm classification for computed tomography, Vascular/biliary involvement, Extrahepatic manifestation, XUUB project

Core tip: This study demonstrates for the first time how different computed tomography morphological types of liver lesions in alveolar echinococcosis (AE) affect the intrahepatic involvement pattern as well as distant extrahepatic disease manifestations. The disease shows different characteristics in an intercontinental comparison between Europe and China. These results may provide information about the behavior of this disease during its initial manifestation and its progression. A morphological classification of AE liver lesions seems therefore not only useful in order to facilitate the initial differential diagnosis but also indicates a direct clinical impact.