Unraveling the relationship among inflammatory responses, oxidative damage, and host susceptibility to Opisthorchis viverrini infection: A comparative analysis in animal models

Vet World Vol.16 November-2023 Article-17

Research Article

Veterinary World, 16(11): 2303-2312

https://doi.org/10.14202/vetworld.2023.2303-2312

Sirikachorn Tangkawattana^1,2, Watcharapol Suyapoh³, Nathamon Taiki⁴, Paramin Tookampee⁴, Ravisara Chitchak⁴, Theerayut Thongrin⁵, and Prasarn Tangkawattana¹

1. Department of Veterinary Pathobiology, Faculty of Veterinary Medicine, Khon Kaen University, Khon Kaen, Thailand.
2. WHO Collaborating Centre for Research and Control of Opisthorchiasis (Southeast Asian Liver Fluke Disease), Tropical Disease Research Center, Khon Kaen University, Khon Kaen, Thailand.
3. Department of Veterinary Science, Faculty of Veterinary Science, Prince of Songkla University, Songkhla, Thailand.
4. Doctor of Veterinary Medicine Program, Faculty of Veterinary Medicine, Khon Kaen University, Thailand.
5. Master of Science Program in Veterinary Science, Faculty of Veterinary Medicine, Khon Kaen University, Thailand.

Background and Aim: Opisthorchis viverrini infection-induced inflammation contributes to cholangiocarcinoma (CCA) development in humans and animals. Inflammation generates free radicals, such as reactive oxygen species and reactive nitrogen species (RNS), which damage the host’s DNA. However, only 5% of O. viverrini-infected individuals develop malignancy, suggesting that variations in the inflammatory response of individuals to the parasite may influence susceptibility. Due to limitations in studying human susceptibility, we used an animal model to investigate the profiles of inflammatory reactions, oxidative burst, and irreversible DNA damage. This study aimed to explore the potential role of inflammation and RNS in causing DNA damage that may predispose susceptible hosts and non-susceptible animal models to cancer development in O. viverrini infection.

Materials and Methods: This experimental study was conducted on 30 Syrian golden hamsters (OV-H) and 30 BALB/c mice (OV-M) infected with O. viverrini, representing susceptible and non-susceptible models, respectively. Five animals per group were examined at six predetermined time points during the experiment. Biliary tract samples were systematically investigated using histopathological evaluation for inflammatory cell infiltration and immunohistochemical staining for RNS production and markers of DNA damage, including nitrotyrosine and 8-hydroxy-2ʹ-deoxyguanosine. These features were quantified and compared among the experimental groups. Mann–Whitney U-test was used for statistical analysis, with p < 0.05 considered statistically significant.

Results: The comparison revealed that the OV-M group exhibited significantly earlier and higher rates of inflammatory cell infiltration during the acute phase, whereas the OV-H group exhibited chronic and more severe inflammation (p < 0.020). Intracellular RNS production and DNA damage were closely associated with the inflammatory response.

Conclusion: This study demonstrates differential responses in susceptible and non-susceptible models of O. viverrini infection regarding disease onset and duration, as well as intracellular RNS production and DNA damage caused by inflammation. Persistent inflammation generated oxidatively damaged DNA, which is a distinct pathological characteristic of susceptible hosts and may be critical for CCA development. Keywords: cholangiocarcinoma, DNA damage, inflammatory reactions, Syrian golden hamsters.

Keywords: cholangiocarcinoma, DNA damage, inflammatory reactions, Syrian golden hamsters.

How to cite this article: Tangkawattana S, Suyapoh W, Taiki N, Tookampee P, Chitchak R, Thongrin T, and Tangkawattana P (2023) Unraveling the relationship among inflammatory responses, oxidative damage, and host susceptibility to Opisthorchis viverrini infection: A comparative analysis in animal models, Veterinary World, 16(11): 2303-2312.

Received: 10-06-2023 Accepted: 16-10-2023 Published online: 19-11-2023

Corresponding author: Sirikachorn Tangkawattana E-mail: sirikach@kku.ac.th

DOI: 10.14202/vetworld.2023.2303-2312

Copyright: Tangkawattana, et al. This article is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.