Infection with Opisthorchis felineus induces intraepithelial neoplasia of the biliary tract in a rodent model

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Abstract

The findings of this report support the inclusion of infection with Opisthorchis felineus among the Group 1 biological carcinogens. Oxysterol-like metabolites of liver fluke origin and the occurrence of biliary intraepithelial neoplasia (BilIN) in liver fluke-infected hamsters support this interpretation. The liver fluke Opisthorchis felineus is a member of the triad of epidemiologically relevant species of the trematode family Opisthorchiidae, and the causative agent of opisthorchiasis felinea over an extensive range that spans regions of Eurasia. The International Agency for Research on Cancer classifies the infection with the liver flukes Opisthorchis viverrini and Clonorchis sinensis as group 1 agents and a major risk factor for cholangiocarcinoma. However, the carcinogenic potential of the infection with O. felineus is less clear. Here, we present findings that support the inclusion of O. felineus in the Group 1 list of biological carcinogens. Two discrete lines of evidence support the notion that infection with this liver fluke is carcinogenic. First, novel oxysterol-like metabolites detected by liquid chromatography-mass spectroscopy in the egg and adult developmental stages of O. felineus, and in bile, sera, and urine of liver fluke-infected hamsters exhibited marked similarity to oxysterol-like molecules known from O. viverrini. Numerous oxysterols and related DNA-adducts detected in the liver fluke eggs and in bile from infected hamsters suggested that infection-associated oxysterols induced chromosomal lesions in host cells. Second, histological analysis of liver sections from hamsters infected with O. felineus confirmed portal area enlargement, inflammation with severe periductal fibrosis and changes in the epithelium of the biliary tract characterized as biliary intraepithelial neoplasia, BilIN. The consonance of these biochemical and histopathological changes revealed that O. felineus infection in this rodent model induced precancerous lesions conducive to malignancy.

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The tumorigenic liver fluke Opisthorchis viverrini--multiple pathways to cancer.

Banchob Sripa, Paul Brindley, Jason Mulvenna … (2012)

Liver fluke infection caused by Opisthorchis viverrini is a major public health problem in Thailand and adjacent countries. In addition to infection-associated morbidity, infection with O. viverrini and the related Clonorchis sinensis are unarguable risk factors for cholangiocarcinoma (CAA, bile-duct cancer). Here we review the pathogenesis of opisthorchiasis and the association between O. viverrini infection and bile-duct cancer, focusing on the molecular parallels between wound healing, chronic inflammation, and cancer development. We review a schema for human disease progression from fluke infection, chronic opisthorchiasis, advanced periductal fibrosis, and cholangiocarcinogenesis, and present a rationale for biomarker discovery to facilitate early intervention. We conclude by addressing post-genomic advances with a view to developing new control strategies to combat this infectious cancer. Copyright © 2012 Elsevier Ltd. All rights reserved.

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Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis.

Yusuke Hiraku, Ning Ma, Somchai Pinlaor … (2006)

Infection and chronic inflammation are proposed to contribute to carcinogenesis through inflammation-related mechanisms. Infection with hepatitis C virus, Helicobacter pylori and the liver fluke, Opisthorchis viverrini (OV), are important risk factors for hepatocellular carcinoma (HCC), gastric cancer and cholangiocarcinoma, respectively. Inflammatory bowel diseases (IBDs) and oral diseases, such as oral lichen planus (OLP) and leukoplakia, are associated with colon carcinogenesis and oral squamous cell carcinoma (OSCC), respectively. We performed a double immunofluorescence labeling study and found that nitrative and oxidative DNA lesion products, 8-nitroguanine and 8-oxo-7,8-dihydro-2'-deoxyguanosine (8-oxodG), were formed and inducible nitric oxide synthase (iNOS) was expressed in epithelial cells and inflammatory cells at the site of carcinogenesis in humans and animal models. Antibacterial, antiviral and antiparasitic drugs dramatically diminished the formation of these DNA lesion markers and iNOS expression. These results suggest that oxidative and nitrative DNA damage occurs at the sites of carcinogenesis, regardless of etiology. Therefore, it is considered that excessive amounts of reactive nitrogen species produced via iNOS during chronic inflammation may play a key role in carcinogenesis by causing DNA damage. On the basis of our results, we propose that 8-nitroguanine is a promising biomarker to evaluate the potential risk of inflammation-mediated carcinogenesis.

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Biliary intraepithelial neoplasia: an international interobserver agreement study and proposal for diagnostic criteria.

Jens Van Lier, Hironori Haga, Cynthia L Ferrell … (2007)

Cholangiocarcinoma of the intrahepatic and extrahepatic bile ducts develops through a multistep histopathologic sequence. Premalignant or non-invasive neoplastic lesions of bile ducts have been historically called biliary dysplasia or atypical biliary epithelium. To this date, no standard terminology or classification system has been offered for these lesions. In 2005, a conceptual framework and diagnostic criteria for biliary intraepithelial neoplasia (BilIN) were proposed using the livers of patients with hepatolithiasis. We report herein an international interobserver agreement study on the diagnosis of biliary non-invasive neoplastic lesions with the goal to obtain a consensus on the terminology and grading. Seventeen pathologists from the United States, Europe and Asia participated in this study. They shared a digital file containing histological pictures of 30 foci of non-invasive neoplastic lesions selected from the biliary system of patients suffering from primary sclerosing cholangitis, choledochal cyst or hepatolithiasis. In the criteria, we proposed in 2005, BilIN was classified into three categories based on the degree of atypia: BilIN-1, BilIN-2 and BilIN-3. In this study, consensus was reached for the terminology of BilIN and the three-grade classification system. Interobserver agreement on the diagnosis was moderate (kappa-value=0.45). On the basis of the suggestions and opinions obtained from the 17 participants, the original criteria for BilIN were revised. We now propose a new consensus classification of BilIN that may assist in allowing a more uniform terminology for the diagnosis of biliary non-invasive neoplastic lesions. This classification should help to advance clinical and research applications.

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Author and article information

Journal

Title: Carcinogenesis

Publisher: Oxford University Press (OUP)

ISSN (Print): 0143-3334

ISSN (Electronic): 1460-2180

Publication date Created: September 2017

Publication date Created: September 01 2017

Publication date Created: May 10 2017

Publication date Other: September 2017

Publication date (Print): September 01 2017

Publication date (Electronic): May 10 2017

Volume: 38

Issue: 9

Pages: 929-937

Affiliations

[1 ] Center for the Study in Animal Science, ICETA, University of Porto, Rua de D. Manuel II, Apt 55142, 4051–401 Porto, Portugal,

[2 ] UCBIO/REQUIMTE, Department of Chemistry and Biochemistry, Faculty of Sciences, University of Porto, Rua do Campo Alegre 687, 4169-007 Porto, Portugal,

[3 ] Laboratory of Molecular Mechanisms of Pathological Processes, Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, 10 Lavrentiev Avenue, 630090 Novosibirsk, Russia,

[4 ] Novosibirsk State University, 2 Pirogov Street, 630090 Novosibirsk, Russia,

[5 ] Department of Parasitology,

[6 ] Department of Pathology,

[7 ] Tropical Diseases Research Laboratory, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;

[8 ] Department of Microbiology, Immunology & Tropical Medicine, Research Center for Neglected Diseases of Poverty, School of Medicine & Health Sciences, George Washington University, Washington, DC 20037, USA;

[9 ] Laboratory of Drug Metabolism and Pharmacokinetics, Institute of Molecular Biology and Biophysics, 2/12 Tymakov Street, 630055 Novosibirsk, Russia;

[10 ] Experimental Pathology and Therapeutics Group, Research Center of Instituto Português de Oncologia, Rua Dr. António de Almeida 4200-072 Porto, Portugal;

[11 ] Centre for Parasite Immunology and Biology, Infectious Diseases Department, INSA, Rua Alexandre Herculano 321, 4000–055 Porto, Portugal;

[12 ] Laboratory of Pharmacology, Department of Drug Sciences, Faculty of Pharmacy, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313, Porto, Portugal

Article

DOI: 10.1093/carcin/bgx042

PMC ID: 5862325

PubMed ID: 28910999

SO-VID: 7d3e0423-cc48-4c6a-8a47-8eabcef0a1ac

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Infection with Opisthorchis felineus induces intraepithelial neoplasia of the biliary tract in a rodent model

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Abstract

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Decoding Infection and Transmission

Most cited references 29

The tumorigenic liver fluke Opisthorchis viverrini--multiple pathways to cancer.

Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis.

Biliary intraepithelial neoplasia: an international interobserver agreement study and proposal for diagnostic criteria.

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