Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-20T03:40:27.508Z Has data issue: false hasContentIssue false

Does Opisthorchis viverrini circulate between humans and domestic cats in an endemic area in Thailand?

Published online by Cambridge University Press:  10 May 2022

Pornphutthachat Sota
Affiliation:
Graduate School, Khon Kaen University, Khon Kaen 40002, Thailand WHO Collaborating Center for Research and Control of Opisthorchiasis (Southeast Asian Liver Fluke Disease), Tropical Disease Research Center, Khon Kaen University, Khon Kaen 40002, Thailand
Sutas Suttiprapa*
Affiliation:
WHO Collaborating Center for Research and Control of Opisthorchiasis (Southeast Asian Liver Fluke Disease), Tropical Disease Research Center, Khon Kaen University, Khon Kaen 40002, Thailand Tropical Medicine International Program, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Sirikachorn Tangkawattana
Affiliation:
WHO Collaborating Center for Research and Control of Opisthorchiasis (Southeast Asian Liver Fluke Disease), Tropical Disease Research Center, Khon Kaen University, Khon Kaen 40002, Thailand Faculty of Veterinary Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Manop Sripa
Affiliation:
WHO Collaborating Center for Research and Control of Opisthorchiasis (Southeast Asian Liver Fluke Disease), Tropical Disease Research Center, Khon Kaen University, Khon Kaen 40002, Thailand
David Blair
Affiliation:
College of Science and Engineering, James Cook University, Townsville, Queensland 4811, Australia
Banchob Sripa
Affiliation:
WHO Collaborating Center for Research and Control of Opisthorchiasis (Southeast Asian Liver Fluke Disease), Tropical Disease Research Center, Khon Kaen University, Khon Kaen 40002, Thailand Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
*
Author for correspondence: Sutas Suttiprapa, E-mail: [email protected]

Abstract

The liver fluke Opisthorchis viverrini is a foodborne trematode that, in chronic infection, is a leading cause of bile-duct cancer – cholangiocarcinoma. Cats and dogs are acknowledged as reservoir hosts of this parasite. However, this assumption is based on morphological similarity of flukes recovered from these hosts, without any molecular genetic evidence. The aim of this study was to obtain molecular data from O. viverrini eggs present in feces of humans and cats in the same locality in Thanya sub-district, Kalasin, Thailand. The mitochondrial cytochrome c oxidase subunit 1 (cox1) gene was used as the marker for a population-genetic study. A DNA fragment of the cox1 gene was amplified from stool samples and subjected to nucleotide sequencing. Phylogenetic and haplotype network analyses were performed. The cox1 sequences of O. viverrini eggs from humans and cats largely formed separate clades on the phylogenetic trees, with an Fst value of 0.64 (P < 0.05), indicating largely distinct populations in the 2 species. However, 5 samples from cats were placed in the human cluster and 1 sample from a human was placed in the cat cluster. This suggests that host specificity of ‘human’ and ‘cat’ clades is not absolute. These results indicate that there are 2 populations of O. viverrini, one circulates primarily in humans and the other in cats. However, cross-transmission can occur between these 2 hosts. Taken altogether, the population-genetic evidence from this study partially supports the assumption that the cat can act as a reservoir host of O. viverrini.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anamnart, W, Intapan, PM and Maleewong, W (2013) Modified formalin-ether concentration technique for diagnosis of human strongyloidiasis. The Korean Journal of Parasitology 51, 743.10.3347/kjp.2013.51.6.743CrossRefGoogle ScholarPubMed
Boonmars, T, Boonjaraspinyo, S and Kaewsamut, B (2009) Animal models for Opisthorchis viverrini infection. Parasitology Research 104, 701703.10.1007/s00436-008-1268-xCrossRefGoogle ScholarPubMed
Buathong, S, Leelayoova, S, Mungthin, M, Ruang-areerate, T, Naaglor, T, Suwannahitatorn, P, Piyaraj, P, Taamasri, P and Tan-ariya, P (2017) Molecular discrimination of Opisthorchis-like eggs from residents in a rural community of central Thailand. PLoS Neglected Tropical Diseases 11, 117.10.1371/journal.pntd.0006030CrossRefGoogle Scholar
Cai, XQ, Liu, GH, Song, HQ, Wu, CY, Zou, FC, Yan, HK, Yuan, ZG, Lin, RQ and Zhu, XQ (2012) Sequences and gene organization of the mitochondrial genomes of the liver flukes Opisthorchis viverrini and Clonorchis sinensis (Trematoda). Parasitology Research 110, 235243.10.1007/s00436-011-2477-2CrossRefGoogle ScholarPubMed
Crellen, T, Sithithaworn, P, Pitaksakulrat, O, Khuntikeo, N, Medley, GF and Hollingsworth, TD (2021) Towards evidence-based control of Opisthorchis viverrini. Trends in Parasitology 37, 370380.10.1016/j.pt.2020.12.007CrossRefGoogle ScholarPubMed
Echaubard, P, Sripa, B, Mallory, FF and Wilcox, BA (2016) The role of evolutionary biology in research and control of liver flukes in Southeast Asia. Infection, Genetics and Evolution 43, 381397.10.1016/j.meegid.2016.05.019CrossRefGoogle ScholarPubMed
Excoffier, L, Laval, G and Schneider, S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1, 4750.10.1177/117693430500100003CrossRefGoogle Scholar
Haonon, O, Liu, Z, Dangtakot, R, Intuyod, K, Pinlaor, P, Puapairoj, A, Cha'On, U, Sengthong, C, Pongking, T, Onsurathum, S, Yingklang, M, Phetcharaburanin, J, Li, JV and Pinlaor, S (2021) Opisthorchis viverrini infection induces metabolic and fecal microbial disturbances in association with liver and kidney pathologies in hamsters. Journal of Proteome Research 20, 39403951.10.1021/acs.jproteome.1c00246CrossRefGoogle ScholarPubMed
Kaewkes, S (2003) Taxonomy and biology of liver flukes. Acta Tropica 88, 177186.10.1016/j.actatropica.2003.05.001CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.10.1093/molbev/msw054CrossRefGoogle ScholarPubMed
Leigh, JW and Bryant, D (2015). Popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 11101116.10.1111/2041-210X.12410CrossRefGoogle Scholar
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.10.1093/bioinformatics/btp187CrossRefGoogle ScholarPubMed
Namsanor, J, Pitaksakulrat, O, Kopolrat, K, Kiatsopit, N, Webster, BL, Gower, CM, Webster, JP, Laha, T, Saijuntha, W, Laoprom, N, Andrews, RH, Petney, TN, Blair, D and Sithithaworn, P (2020) Impact of geography and time on genetic clusters of Opisthorchis viverrini identified by microsatellite and mitochondrial DNA analysis. International Journal for Parasitology 50, 11331144.10.1016/j.ijpara.2020.06.011CrossRefGoogle ScholarPubMed
Nguyen, TTB, Arimatsu, Y, Hong, SJ, Brindley, PJ, Blair, D, Laha, T and Sripa, B (2015) Genome-wide characterization of microsatellites and marker development in the carcinogenic liver fluke Clonorchis sinensis. Parasitology Research 114, 22632272.10.1007/s00436-015-4419-xCrossRefGoogle ScholarPubMed
Petney, TN, Andrews, RH, Saijuntha, W, Tesana, S, Prasopdee, S, Kiatsopit, N and Sithithaworn, P (2018) Taxonomy, ecology and population genetics of Opisthorchis viverrini and its intermediate hosts. Advances in Parasitology 101, 139.10.1016/bs.apar.2018.05.001CrossRefGoogle ScholarPubMed
Pitaksakulrat, O, Webster, BL, Webster, JP, Laha, T, Saijuntha, W, Lamberton, PHL, Kiatsopit, N, Andrews, RH, Petney, TN and Sithithaworn, P (2018) Phylogenetic relationships within the Opisthorchis viverrini species complex with specific analysis of O. viverrini sensu lato from Sakon Nakhon, Thailand by mitochondrial and nuclear DNA sequencing. Infection, Genetics and Evolution 62, 8694.10.1016/j.meegid.2018.04.022CrossRefGoogle Scholar
Saijuntha, W, Sithithaworn, P, Wongkham, S, Laha, T, Pipitgool, V, Tesana, S, Chilton, NB, Petney, TN and Andrews, RH (2007) Evidence of a species complex within the food-borne trematode Opisthorchis viverrini and possible co-evolution with their first intermediate hosts. International Journal for Parasitology 37, 695703.10.1016/j.ijpara.2006.12.008CrossRefGoogle ScholarPubMed
Saijuntha, W, Sithithaworn, P, Wongkham, S, Laha, T, Chilton, NB, Petney, TN, Barton, M and Andrews, RH (2008) Mitochondrial DNA sequence variation among geographical isolates of Opisthorchis viverrini in Thailand and Lao PDR, and phylogenetic relationships with other trematodes. Parasitology 135, 14791486.10.1017/S0031182008005015CrossRefGoogle ScholarPubMed
Sanpool, O, Aung, WPP, Rodpai, R, Maleewong, W and Intapan, PM (2018) Human liver fluke Opisthorchis viverrini (Trematoda, Opisthorchiidae) in Central Myanmar: new records of adults and metacercariae identified by morphology and molecular analysis. Acta Tropica 185, 149155.10.1016/j.actatropica.2018.05.009CrossRefGoogle ScholarPubMed
Sithithaworn, P, Andrews, RH, Petney, TN, Saijuntha, W and Laoprom, N (2012) The systematics and population genetics of Opisthorchis viverrini sensu lato: implications in parasite epidemiology and bile duct cancer. Parasitology International 61, 3237.10.1016/j.parint.2011.07.020CrossRefGoogle ScholarPubMed
Sithithaworn, P, Yongvanit, P, Duenngai, K, Kiatsopit, N and Pairojkul, C (2014) Roles of liver fluke infection as risk factor for cholangiocarcinoma. Journal of Hepato-Biliary-Pancreatic Sciences 21, 301308.10.1002/jhbp.62CrossRefGoogle ScholarPubMed
Sripa, B, Suwannatrai, AT, Sayasone, S, Do, DT, Khieu, V and Yang, Y (2021) Current status of human liver fluke infections in the Greater Mekong Subregion. Acta Tropica 224, 106133.10.1016/j.actatropica.2021.106133CrossRefGoogle ScholarPubMed
Tangkawattana, S and Tangkawattana, P (2018) Reservoir animals and their roles in transmission of Opisthorchis viverrini. Advances in Parasitology 101, 6995.10.1016/bs.apar.2018.05.003CrossRefGoogle ScholarPubMed
Thaenkham, U, Nuamtanong, S, Vonghachack, Y, Yoonuan, T, Sanguankiat, S, Dekumyoy, P, Prommasack, B, Kobayashi, J and Waikagul, J (2011) Discovery of Opisthorchis lobatus (Trematoda: Opisthorchiidae): a new record of small liver flukes in the greater Mekong sub-region. Journal of Parasitology 97, 11521158.10.1645/GE-2764.1CrossRefGoogle ScholarPubMed
Supplementary material: File

Sota et al. supplementary material

Sota et al. supplementary material 1

Download Sota et al. supplementary material(File)
File 20.9 KB
Supplementary material: File

Sota et al. supplementary material

Sota et al. supplementary material 2

Download Sota et al. supplementary material(File)
File 19.1 KB
Supplementary material: File

Sota et al. supplementary material

Sota et al. supplementary material 3

Download Sota et al. supplementary material(File)
File 16.6 KB
Supplementary material: File

Sota et al. supplementary material

Sota et al. supplementary material 4

Download Sota et al. supplementary material(File)
File 465 KB
Supplementary material: File

Sota et al. supplementary material

Sota et al. supplementary material 5

Download Sota et al. supplementary material(File)
File 24.4 KB