Opisthorchiasis and the Microbiome

Bile; Liver fluke; Microbiome; Microbiota; Opisthorchiasis; Aggregatibacter; Article; Erysipelotrichaceae; Eubacteriaceae; Fasciola hepatica; Helicobacter infection; Helicobacter pylori; Klebsiella; Lachnospiraceae; Lactobacillaceae; Lactobacillus; Opisthorchis felineus; Opisthorchis viverrini; Porphyromonadaceae; Ruminococcaceae; Treponema; Animals; Biodiversity; Disease Models, Animal; Humans

Abstract :

[en] The liver flukes Opisthorchis viverrini, O. felineus, and Clonorchis sinensis are closely related fish-borne trematodes endemic in East Asia, Eurasia, and Siberia. Following ingestion, the parasites locate to the biliary tree, where chronic infection frequently leads to cholangiocarcinoma (CCA). Infection with C. sinensis or O. viverrini is classified as a Group 1 carcinogen by the International Agency for Research on Cancer. Infection with O. felineus may also be carcinogenic. The mechanism(s) by which infection with these liver flukes culminates in CCA remain elusive, although they are likely to be multi-factorial. Not yet well studied is the influence of opisthorchiasis on the microbiome of the host despite reports that helminth parasites are capable of affecting the microbiome, potentially modulating gastrointestinal inflammation in response to the appearance of pathogenic strains of bacteria. Here, we review recent findings related to opisthorchiasis and the microbiome and related issues. In the hamster, a tractable model of infection with liver fluke and of infection-induced biliary morbidity and CCA, infection with O. viverrini perturbs the microbiome of the gastrointestinal tract, including increasing numbers of Lachnospiraceae, Ruminococcaceae, Lactobacillaceae, and others, while decreasing Porphyromonadaceae, Erysipelotrichaceae, and Eubacteriaceae. In addition, a complex microbial community associates with the parasites within the biliary tree, including Helicobacter pylori and related bacteria. Moreover, higher rates of infection with Helicobacter occur in Thailand in persons with opisthorchiasis in a liver fluke infection intensity-dependent manner. Experimental infection of hamsters with Opisthorchis felineus results in increased alpha diversity of the microbiota diversity in the biliary tract. In humans, infection with O. felineus modifies the composition of the biliary microbiome, with increasing numbers of species of Klebsiella, Aggregatibacter, Lactobacillus, Treponema, and others. Several phylotypes of Archaea occurred solely in bile from persons infected with O. felineus. © 2018 Elsevier Ltd

Disciplines :

Immunology & infectious disease

Author, co-author :

Saltykova, I. V.; Siberian State Medical University, Central Research Laboratory, Tomsk, Russian Federation

Petrov, Viacheslav ; Siberian State Medical University (SSMU), 2, Moscow Trakt, Tomsk, 634050, Russian Federation

Brindley, P. J.; Department of Microbiology, Immunology & Tropical Medicine, Research Center for Neglected Diseases of Poverty, School of Medicine & Health Sciences, George Washington University, Washington, DC, United States

Language :

English

Title :

Opisthorchiasis and the Microbiome

Publication date :

2018

Journal title :

Advances in Parasitology

ISSN :

0065-308X

Publisher :

Academic Press

Volume :

102

Pages :

1-23

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

NIH - National Institutes of Health [US-MD] [US-MD]
NCI - National Cancer Institute [US-MD] [US-MD]
NIAID - National Institute of Allergy and Infectious Diseases [US-MD] [US-MD]
NCI - National Computational Infrastructure [AU]
RSF - Russian Science Foundation [RU]

Commentary :

9780128151914

Available on ORBi :

since 27 May 2021

Statistics

Number of views

34 (3 by ULiège)

Number of downloads

1 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Bataller, R., Brenner, D.A., Liver fibrosis (2005) J. Clin. Investig., 115, pp. 209-218
Begley, M., Gahan, C.G., Hill, C., The interaction between bacteria and bile (2005) FEMS Microbiol. Rev., 29, pp. 625-651
Bhamarapravati, N., Thammavit, W., Vajrasthira, S., Liver changes in hamsters infected with a liver fluke of man, Opisthorchis viverrini (1978) Am. J. Trop. Med. Hyg., 27, pp. 787-794
Boonyanugomol, W., Chomvarin, C., Sripa, B., Bhudhisawasdi, V., Khuntikeo, N., Hahnvajanawong, C., Chamsuwan, A., Helicobacter pylori in Thai patients with cholangiocarcinoma and its association with biliary inflammation and proliferation (2012) HPB, 14, pp. 177-184
Broadhurst, M.J., Ardeshir, A., Kanwar, B., Mirpuri, J., Gundra, U.M., Leung, J.M., Wiens, K.E., Yarovinsky, F., Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon (2012) PLoS Pathog., 8, p. e1003000
Calvopina, M., Cevallos, W., Kumazawa, H., Eisenberg, J., High prevalence of human liver infection by Amphimerus spp. flukes, Ecuador (2011) Emerg. Infect. Dis., 17, pp. 2331-2334
Carpenter, H.A., Bacterial and parasitic cholangitis (1998) Mayo Clin. Proc., 73, pp. 473-478
Chand, D., Panigrahi, P., Varshney, N., Ramasamy, S., Suresh, C.G., Structure and function of a highly active Bile Salt Hydrolase (BSH) from Enterococcus faecalis and post-translational processing of BSH enzymes (2018) Biochim. Biophys. Acta, 1866, pp. 507-518
Chng, K.R., Chan, S.H., Ng, A.H.Q., Li, C., Jusakul, A., Bertrand, D., Wilm, A., Lim, K.H., Tissue microbiome profiling identifies an enrichment of specific enteric bacteria in Opisthorchis viverrini associated cholangiocarcinoma (2016) EBioMedicine, 8, pp. 195-202
Cooper, P., Walker, A.W., Reyes, J., Chico, M., Salter, S.J., Vaca, M., Parkhill, J., Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota (2013) PLoS One, 8, p. e76573
Dangtakot, R., Pinlaor, S., Itthitaetrakool, U., Chaidee, A., Chomvarin, C., Sangka, A., Wilailuckana, C., Pinlaor, P., Coinfection with Helicobacter pylori and Opisthorchis viverrini enhances the severity of hepatobiliary abnormalities in hamsters (2017) Infect. Immun., 85
Deenonpoe, R., Chomvarin, C., Pairojkul, C., Chamgramol, Y., Loukas, A., Brindley, P.J., Sripa, B., The carcinogenic liver fluke Opisthorchis viverrini is a reservoir for species of Helicobacter (2015) Asian Pac. J. Cancer Prev., 16, pp. 1751-1758
Deenonpoe, R., Mairiang, E., Mairiang, P., Pairojkul, C., Chamgramol, Y., Rinaldi, G., Loukas, A., Sripa, B., Elevated prevalence of Helicobacter species and virulence factors in opisthorchiasis and associated hepatobiliary disease (2017) Sci. Rep., 7, p. 42744
Dheilly, N.M., Bolnick, D., Bordenstein, S., Brindley, P.J., Figueres, C., Holmes, E.C., Martinez Martinez, J., Rosario, K., Parasite microbiome project: systematic investigation of microbiome dynamics within and across parasite-host interactions (2017) mSystems, 2
Dourado, M.N., Andreote, F.D., Dini-Andreote, F., Conti, R., Araujo, J.M., Araujo, W.L., Analysis of 16S rRNA and mxaF genes revealing insights into Methylobacterium niche-specific plant association (2012) Genet. Mol. Biol., 35, pp. 142-148
Dussurget, O., Cabanes, D., Dehoux, P., Lecuit, M., Buchrieser, C., Glaser, P., Cossart, P., European Listeria Genome Consortium, Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis (2002) Mol. Microbiol., 45, pp. 1095-1106
Emerson, D., Fleming, E.J., McBeth, J.M., Iron-oxidizing bacteria: an environmental and genomic perspective (2010) Annu. Rev. Microbiol., 64, pp. 561-583
Fedorova, O.S., Fedotova, M.M., Sokolova, T.S., Golovach, E.A., Kovshirina, Y.V., Ageeva, T.S., Kovshirina, A.E., Odermatt, P., Opisthorchis felineus infection prevalence in Western Siberia: a review of Russian literature (2018) Acta Trop., 178, pp. 196-204
Fedorova, O.S., Kovshirina, Y.V., Kovshirina, A.E., Fedotova, M.M., Deev, I.A., Petrovskiy, F.I., Filimonov, A.V., Saltykova, I.V., Opisthorchis felineus infection and cholangiocarcinoma in the Russian Federation: a review of medical statistics (2017) Parasitol. Int., 66, pp. 365-371
Gendrel, D., Kombila, M., Beaudoin-Leblevec, G., Richard-Lenoble, D., Nontyphoidal salmonellal septicemia in Gabonese children infected with Schistosoma intercalatum (1994) Clin. Infect. Dis., 18, pp. 103-105
Giacomin, P., Zakrzewski, M., Jenkins, T.P., Su, X., Al-Hallaf, R., Croese, J., de Vries, S., Loukas, A., Changes in duodenal tissue-associated microbiota following hookworm infection and consecutive gluten challenges in humans with coeliac disease (2016) Sci. Rep., 6, p. 36797
Guernier, V., Brennan, B., Yakob, L., Milinovich, G., Clements, A.C., Soares Magalhaes, R.J., Gut microbiota disturbance during helminth infection: can it affect cognition and behaviour of children? (2017) BMC Infect. Dis., 17, p. 58
Hooper, L.V., Littman, D.R., Macpherson, A.J., Interactions between the microbiota and the immune system (2012) Science, 336, pp. 1268-1273
Horáčková, Š., Plocková, M., Demnerová, K., (2018) Biotechnol Adv, 36 (3), pp. 682-690. , DOI: 10.1016/j.biotechadv.2017.12.005 pmid:29248683
Humans, I.W.G.O.T.E.O.C.R.T., Biological agents. Volume 100 B. A review of human carcinogens (2012) IARC Monogr. Eval. Carcinog. Risks Hum., 100, pp. 1-441
Imhann, F., Vich Vila, A., Bonder, M.J., Fu, J., Gevers, D., Visschedijk, M.C., Spekhorst, L.M., van Dullemen, H.M., Interplay of host genetics and gut microbiota underlying the onset and clinical presentation of inflammatory bowel disease (2018) Gut, 67, pp. 108-119
Itthitaetrakool, U., Pinlaor, P., Pinlaor, S., Chomvarin, C., Dangtakot, R., Chaidee, A., Wilailuckana, C., Yongvanit, P., Chronic Opisthorchis viverrini infection changes the liver microbiome and promotes Helicobacter growth (2016) PLoS One, 11, p. e0165798
Jarocki, P., Podlesny, M., Glibowski, P., Targonski, Z., A new insight into the physiological role of bile salt hydrolase among intestinal bacteria from the genus Bifidobacterium (2014) PLoS One, 9, p. e114379
Jenkins, T.P., Rathnayaka, Y., Perera, P.K., Peachey, L.E., Nolan, M.J., Krause, L., Rajakaruna, R.S., Cantacessi, C., Infections by human gastrointestinal helminths are associated with changes in faecal microbiota diversity and composition (2017) PLoS One, 12, p. e0184719
Jimenez, E., Sanchez, B., Farina, A., Margolles, A., Rodriguez, J.M., Characterization of the bile and gall bladder microbiota of healthy pigs (2014) Microbiologyopen, 3, pp. 937-949
Kau, A.L., Ahern, P.P., Griffin, N.W., Goodman, A.L., Gordon, J.I., Human nutrition, the gut microbiome and the immune system (2011) Nature, 474, pp. 327-336
Kim, G.B., Miyamoto, C.M., Meighen, E.A., Lee, B.H., Cloning and characterization of the bile salt hydrolase genes (bsh) from Bifidobacterium bifidum strains (2004) Appl. Environ. Microbiol., 70, pp. 5603-5612
Kumar, R., Rajkumar, H., Kumar, M., Varikuti, S.R., Athimamula, R., Shujauddin, M., Ramagoni, R., Kondapalli, N., Molecular cloning, characterization and heterologous expression of bile salt hydrolase (Bsh) from Lactobacillus fermentum NCDO394 (2013) Mol. Biol. Rep., 40, pp. 5057-5066
Kunik, T., Tzfira, T., Kapulnik, Y., Gafni, Y., Dingwall, C., Citovsky, V., Genetic transformation of HeLa cells by Agrobacterium (2001) Proc. Natl. Acad. Sci. U.S.A., 98, pp. 1871-1876
Lapthorne, S., Pereira-Fantini, P.M., Fouhy, F., Wilson, G., Thomas, S.L., Dellios, N.L., Scurr, M., Stanton, C., Gut microbial diversity is reduced and is associated with colonic inflammation in a piglet model of short bowel syndrome (2013) Gut Microb., 4, pp. 212-221
Lee, S.C., Tang, M.S., Lim, Y.A., Choy, S.H., Kurtz, Z.D., Cox, L.M., Gundra, U.M., Blaser, M.J., Helminth colonization is associated with increased diversity of the gut microbiota (2014) PLoS Negl. Trop. Dis., 8, p. e2880
Maluenda, F., Csendes, A., Burdiles, P., Diaz, J., Bacteriological study of choledochal bile in patients with common bile duct stones, with or without acute suppurative cholangitis (1989) Hepato Gastroenterol., 36, pp. 132-135
McNulty, S.N., Tort, J.F., Rinaldi, G., Fischer, K., Rosa, B.A., Smircich, P., Fontenla, S., Hallsworth-Pepin, K., Genomes of Fasciola hepatica from the Americas reveal colonization with Neorickettsia endobacteria related to the agents of Potomac horse and human Sennetsu Fevers (2017) PLoS Genet., 13, p. e1006537
Nagarajan, N., Bertrand, D., Hillmer, A.M., Zang, Z.J., Yao, F., Jacques, P.E., Teo, A.S., Lee, W.H., Whole-genome reconstruction and mutational signatures in gastric cancer (2012) Genome Biol., 13, p. R115
Naugler, W.E., Karin, M., The wolf in sheep's clothing: the role of interleukin-6 in immunity, inflammation and cancer (2008) Trends Mol. Med., 14, pp. 109-119
O'Hara, S.P., Tabibian, J.H., Splinter, P.L., Larusso, N.F., The dynamic biliary epithelia: molecules, pathways, and disease (2013) J. Hepatol., 58, pp. 575-582
Pereira, P., Aho, V., Arola, J., Boyd, S., Jokelainen, K., Paulin, L., Auvinen, P., Farkkila, M., Bile microbiota in primary sclerosing cholangitis: impact on disease progression and development of biliary dysplasia (2017) PLoS One, 12, p. e0182924
Pereira, S.G., Moura, J., Carvalho, E., Empadinhas, N., Microbiota of chronic diabetic wounds: ecology, impact, and potential for innovative treatment strategies (2017) Front. Microbiol., 8, p. 1791
Pershina, A.G., Ivanov, V.V., Efimova, L.V., Shevelev, O.B., Vtorushin, S.V., Perevozchikova, T.V., Sazonov, A.E., Ogorodova, L.M., Magnetic resonance imaging and spectroscopy for differential assessment of liver abnormalities induced by Opisthorchis felineus in an animal model (2017) PLoS Negl. Trop. Dis., 11, p. e0005778
Pershina, A.G., Saltykova, I.V., Ivanov, V.V., Perina, E.A., Demin, A.M., Shevelev, O.B., Buzueva, I.I., Ganebnykh, I.N., Hemozoin “knobs” in Opisthorchis felineus infected liver (2015) Parasites Vectors, 8, p. 459
Petney, T.N., Andrews, R.H., Saijuntha, W., Wenz-Mucke, A., Sithithaworn, P., The zoonotic, fish-borne liver flukes Clonorchis sinensis, Opisthorchis felineus and Opisthorchis viverrini (2013) Int. J. Parasitol., 43, pp. 1031-1046
Plieskatt, J.L., Deenonpoe, R., Mulvenna, J.P., Krause, L., Sripa, B., Bethony, J.M., Brindley, P.J., Infection with the carcinogenic liver fluke Opisthorchis viverrini modifies intestinal and biliary microbiome (2013) FASEB J., 27, pp. 4572-4584
Prakobwong, S., Pinlaor, S., Yongvanit, P., Sithithaworn, P., Pairojkul, C., Hiraku, Y., Time profiles of the expression of metalloproteinases, tissue inhibitors of metalloproteases, cytokines and collagens in hamsters infected with Opisthorchis viverrini with special reference to peribiliary fibrosis and liver injury (2009) Int. J. Parasitol., 39, pp. 825-835
Prakobwong, S., Yongvanit, P., Hiraku, Y., Pairojkul, C., Sithithaworn, P., Pinlaor, P., Pinlaor, S., Involvement of MMP-9 in peribiliary fibrosis and cholangiocarcinogenesis via Rac1-dependent DNA damage in a hamster model (2010) Int. J. Cancer, 127, pp. 2576-2587
Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Shen, D., A metagenome-wide association study of gut microbiota in type 2 diabetes (2012) Nature, 490, pp. 55-60
Razumilava, N., Gores, G.J., Classification, diagnosis, and management of cholangiocarcinoma (2013) Clin. Gastroenterol. Hepatol., 11. , 13-21 e1 1
quiz e13–14
Saltykova, I.V., Petrov, V.A., Dorofeeva Yu, B., Ivanov, V.V., Sazonov, A.E., Hemozoin Accumulation Associated with Opisthorchis felineus Infection and the Analysis of Its Role in Changing the Bile Ducts Microbiota (2017), pp. 70-78. , Vestnik Baltiyskogo Federalnogo Universiteta Kanta, Section of Natural and Medical Science
Saltykova, I.V., Petrov, V.A., Logacheva, M.D., Ivanova, P.G., Merzlikin, N.V., Sazonov, A.E., Ogorodova, L.M., Brindley, P.J., Biliary microbiota, gallstone disease and infection with Opisthorchis felineus (2016) PLoS Negl. Trop. Dis., 10, p. e0004809
Sauter, C., Is Hodgkin's disease a human counterpart of bacterially induced crown-gall tumours? (1995) Lancet, 346, p. 1433
Schloissnig, S., Arumugam, M., Sunagawa, S., Mitreva, M., Tap, J., Zhu, A., Waller, A., Martin, J., Genomic variation landscape of the human gut microbiome (2013) Nature, 493, pp. 45-50
Schwabe, R.F., Jobin, C., The microbiome and cancer (2013) Nat. Rev. Cancer, 13, pp. 800-812
Segura-Lopez, F.K., Guitron-Cantu, A., Torres, J., Association between Helicobacter spp. infections and hepatobiliary malignancies: a review (2015) World J. Gastroenterol., 21, pp. 1414-1423
Shin, H.R., Oh, J.K., Masuyer, E., Curado, M.P., Bouvard, V., Fang, Y.Y., Wiangnon, S., Hong, S.T., Epidemiology of cholangiocarcinoma: an update focusing on risk factors (2010) Cancer Sci., 101, pp. 579-585
Sobhani, I., Tap, J., Roudot-Thoraval, F., Roperch, J.P., Letulle, S., Langella, P., Corthier, G., Furet, J.P., Microbial dysbiosis in colorectal cancer (CRC) patients (2011) PLoS One, 6 (1), p. e16393
Sripa, B., Pathobiology of opisthorchiasis: an update (2003) Acta Trop., 88, pp. 209-220
Sripa, B., Bethony, J.M., Sithithaworn, P., Kaewkes, S., Mairiang, E., Loukas, A., Mulvenna, J., Brindley, P.J., Opisthorchiasis and Opisthorchis-associated cholangiocarcinoma in Thailand and Laos (2011) Acta Trop., 120, pp. S158-S168
Sripa, B., Brindley, P.J., Mulvenna, J., Laha, T., Smout, M.J., Mairiang, E., Bethony, J.M., Loukas, A., The tumorigenic liver fluke Opisthorchis viverrini–multiple pathways to cancer (2012) Trends Parasitol., 28, pp. 395-407
Sripa, B., Kaewkes, S., Sithithaworn, P., Mairiang, E., Laha, T., Smout, M., Pairojkul, C., Thinkamrop, B., Liver fluke induces cholangiocarcinoma (2007) PLoS Med., 4, p. e201
Sripa, B., Mairiang, E., Thinkhamrop, B., Laha, T., Kaewkes, S., Sithithaworn, P., Tessana, S., Bethony, J.M., Advanced periductal fibrosis from infection with the carcinogenic human liver fluke Opisthorchis viverrini correlates with elevated levels of interleukin-6 (2009) Hepatology, 50, pp. 1273-1281
Sripa, B., Thinkhamrop, B., Mairiang, E., Laha, T., Kaewkes, S., Sithithaworn, P., Periago, M.V., Mulvenna, J., Elevated plasma IL-6 associates with increased risk of advanced fibrosis and cholangiocarcinoma in individuals infected by Opisthorchis viverrini (2012) PLoS Negl. Trop. Dis., 6, p. e1654
Tajiri, T., Yoshida, H., Mamada, Y., Taniai, N., Yokomuro, S., Mizuguchi, Y., Diagnosis and initial management of cholangiocarcinoma with obstructive jaundice (2008) World J. Gastroenterol., 14, pp. 3000-3005
Tanaka, H., Hashiba, H., Kok, J., Mierau, I., Bile salt hydrolase of Bifidobacterium longum-biochemical and genetic characterization (2000) Appl. Environ. Microbiol., 66, pp. 2502-2512
Vaughan, J.A., Tkach, V.V., Greiman, S.E., Neorickettsial endosymbionts of the digenea: diversity, transmission and distribution (2012) Adv. Parasitol., 79, pp. 253-297
Verdier, J., Luedde, T., Sellge, G., Biliary mucosal barrier and microbiome (2015) Viszeralmedizin, 31, pp. 156-161
Weinstock, J.V., Autoimmunity: the worm returns (2012) Nature, 491, pp. 183-185
Yoon, S., Yu, J., McDowell, A., Kim, S.H., You, H.J., Ko, G., Bile salt hydrolase-mediated inhibitory effect of Bacteroides ovatus on growth of Clostridium difficile (2017) J. Microbiol., 55, pp. 892-899
Zvonareva, O., Odermatt, P., Golovach, E.A., Fedotova, M.M., Kovshirina, Y.V., Kovshirina, A.E., Kobyakova, O.S., Fedorova, O.S., Life by the river: neglected worm infection in Western Siberia and pitfalls of a one-size-fits-all control approach (2017) Critical Public Health