The impact of Opisthorchis felineus infection and praziquantel treatment on the intestinal microbiota in children

Children; Gut microbiota; Opisthorchis felineus; Parasite; RNA 16S; RNA; Anaerosporobacter; Article; Bacteroides; Barnesiella; Blautia; Escherichia; Eubacterium eligens; Eubacterium hallii; Faecalitalea; Lachnospira; Megasphaera; Oscillibacter; RNA gene; Roseburia; Ruminiclostridium; Shigella; Bacteria (microorganisms); Enterobacteriaceae; Faecalibacterium; Lachnospiraceae; Microbiota; Vermes

Abstract :

[en] The presence of some species of helminths is associated with changes in host microbiota composition and diversity, which varies widely depending on the infecting helminth species and other factors. We conducted a prospective case-control study to evaluate the gut microbiota in children with Opisthorchis felineus infection (n=50) before and after anthelmintic treatment and in uninfected children (n=49) in the endemic region. A total of 99 children and adolescents aged between 7 and 18 years were enrolled to the study. Helminth infection was assessed before and at 3 months after treatment with praziquantel. A complex examination for each participant was performed in the study, including an assessment of the clinical symptoms and an intestinal microbiota survey by 16S rRNA gene sequencing of stool samples. There was no change in alpha diversity between O. felineus-infected and control groups. We found significant changes in the abundances of bacterial taxa at different taxonomic levels between the infected and uninfected individuals. Enterobacteriaceae family was more abundant in infected participants compared to uninfected children. On the genus level, O. felineus-infected participants’ microbiota showed higher levels of Lachnospira, Escherichia-Shigella, Bacteroides, Eubacterium eligens group, Ruminiclostridium 6, Barnesiella, Oscillibacter, Faecalitalea and Anaerosporobacter and reduction of Blautia, Lachnospiraceae FCS020 and Eubacterium hallii group in comparison with the uninfected individuals. Following praziquantel therapy, there were significant differences in abundances of some microorganisms, including an increase of Faecalibacterium and decrease of Megasphaera, Roseburia. Enterobacteriaceae and Escherichia abundances were decreased up to the control group values. Our results highlight the importance of the host-parasite-microbiota interactions for the community health in the endemic regions. © 2021

Disciplines :

Immunology & infectious disease

Author, co-author :

Sokolova, T. S.; Federal State Budget Educational Institution of Higher Education, Siberian State Medical University, Ministry of Healthcare of Russian Federation, Department of Faculty Pediatrics, Moscowsky tract, 2, Tomsk, 634050, Russian Federation

Petrov, Viacheslav ; Siberian State Medical University (SSMU), 2, Moscow Trakt, Tomsk, 634050, Russian Federation ; RECETOX, Masaryk University, Brno, Czech Republic

Saltykova, I. V.; Federal State Budget Educational Institution of Higher Education, Siberian State Medical University, Ministry of Healthcare of Russian Federation, Central Research Laboratory, Tomsk, Russian Federation

Dorofeeva, Y. B.; Federal State Budget Educational Institution of Higher Education, Siberian State Medical University, Ministry of Healthcare of Russian Federation, Biology and genetics department, Tomsk, Russian Federation

Tyakht, A. V.; Center for Precision Genome Editing and Genetic Technologies for Biomedicine, Institute of Gene Biology of Russian Academy of Science, Moscow, Russian Federation, Atlas Biomed Group - Knomics LLC, London, United Kingdom

Ogorodova, L. M.; Federal State Budget Educational Institution of Higher Education, Siberian State Medical University, Ministry of Healthcare of Russian Federation, Department of Faculty Pediatrics, Moscowsky tract, 2, Tomsk, 634050, Russian Federation

Fedorova, O. S.; Federal State Budget Educational Institution of Higher Education, Siberian State Medical University, Ministry of Healthcare of Russian Federation, Department of Faculty Pediatrics, Moscowsky tract, 2, Tomsk, 634050, Russian Federation

Title :

The impact of Opisthorchis felineus infection and praziquantel treatment on the intestinal microbiota in children

Publication date :

2021

Journal title :

Acta Tropica

ISSN :

0001-706X

Publisher :

Elsevier B.V.

Volume :

217

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

Russian Foundation for Basic Research, РФФИ: N19-515-70004

Available on ORBi :

since 27 May 2021

Statistics

Number of views

73 (2 by ULiège)

Number of downloads

113 (3 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Arpaia, N., Campbell, C., Fan, X., Dikiy, S., van der Veeken, J., deRoos, P., Liu, H., Cross, J.R., Pfeffer, K., Coffer, P.J., Rudensky, A.Y., Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504 (2013), 451–455, 10.1038/nature12726.
Barb, J.J., Oler, A.J., Kim, H.S., Chalmers, N., Wallen, G.R., Cashion, A., Munson, P.J., Ames, N.J., Development of an analysis pipeline characterizing multiple hypervariable regions of 16S rRNA using mock samples. PLoS One, 11, 2016, 10.1371/journal.pone.0148047.
Bates, D., Mächler, M., Bolker, B.M., Walker, S.C., Fitting linear mixed-effects models using lme4. J. Stat. Softw., 67, 2015, 10.18637/jss.v067.i01.
Belibasakis, G.N., Öztürk, V.Ö., Emingil, G., Bostanci, N., Synergistetes cluster A in saliva is associated with periodontitis. J. Periodontal Res. 48 (2013), 727–732, 10.1111/jre.12061.
Bolyen, E., Rideout, J.R., Dillon, M.R., Bokulich, N.A., Chase, J., Cope, E.K., Gorlick, K., Keefe, C.R., Keim, P., Kreps, J., Naimey, A.T., Pearson, T., Shiffer, A., Caporaso, J.G., Abnet, C.C., Loftfield, E., Sinha, R., Vogtmann, E., Wan, Y., Al-Ghalith, G.A., Alexander, H., Brown, C.T., Alm, E.J., Duvallet, C., Alm, E.J., Arumugam, M., Brejnrod, A., Rasmussen, L.B., Asnicar, F., Segata, N., Bai, Y., Liu, Y.X., Bai, Y., Liu, Y.X., Bisanz, J.E., Bittinger, K., Brislawn, C.J., Callahan, B.J., Callahan, B.J., Caraballo-Rodríguez, A.M., Silva, D., Dorrestein, R., Ernst, P.C., Gauglitz, M., Jarmusch, J.M., Kang, A.K., Bin, K., Koester, I., Melnik, A.V., Nothias, L.F., Petras, D., Tripathi, A., Wang, M., Caporaso, J.G., Diener, C., Gibbons, S.M., Douglas, G.M., Durall, D.M., Edwardson, C.F., Estaki, M., Fouquier, J., Shaffer, M., Fouquier, J., Lozupone, C., Pruesse, E., Gibbons, S.M., Gibson, D.L., Gonzalez, A., Holste, H., Marotz, C., McDonald, D., Morton, J.T., Navas-Molina, J.A., Song, S.J., Vázquez-Baeza, Y., Xu, Z.Z., Zhu, Q., Knight, R., Guo, J., Hillmann, B., Knights, D., Holmes, S., Holste, H., Huttenhower, C., McIver, L.J., Huttenhower, C., Huttley, G.A., Kaehler, B.D., Janssen, S., Jiang, L., Kang, K.B., Kelley, S.T., Kosciolek, T., Langille, M.G.I., Lee, J., Ley, R., Walters, W., Maher, M., Navas-Molina, J.A., Martin, B.D., Metcalf, J.L., Author correction: reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 (Nature Biotechnology, (2019), 37, 8, (852-857), 10.1038/s41587-019-0209-9). Nat. Biotechnol. 37 (2019), 852–857, 10.1038/s41587-019-0209-9.
Brooks, M., Kristensen, K., Benthem, K., va., Magnusson, A., Berg, C., Nielsen, A., Skaug, H., Mächler, M., Bolker, B., glmmTMB Balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R. J., 9, 2017, 378, 10.32614/RJ-2017-066.
Burisch, J., Pedersen, N., Čuković-Čavka, S., Brinar, M., Kaimakliotis, I., Duricova, D., Shonová, O., Vind, I., Avnstrøm, S., Thorsgaard, N., Andersen, V., Krabbe, S., Dahlerup, J.F., Salupere, R., Nielsen, K.R., Olsen, J., Manninen, P., Collin, P., Tsianos, E.V., Katsanos, K.H., Ladefoged, K., Lakatos, L., Björnsson, E., Ragnarsson, G., Bailey, Y., Odes, S., Schwartz, D., Martinato, M., Lupinacci, G., Milla, M., De Padova, A., D'inca, R., Beltrami, M., Kupcinskas, L., Kiudelis, G., Turcan, S., Tighineanu, O., Mihu, I., Magro, F., Barros, L.F., Goldis, A., Lazar, D., Belousova, E., Nikulina, I., Hernandez, V., Martinez-Ares, D., Almer, S., Zhulina, Y., Halfvarson, J., Arebi, N., Sebastian, S., Lakatos, P.L., Langholz, E., Munkholm, P., East-West gradient in the incidence of inflammatory bowel disease in Europe: the ECCO-EpiCom inception cohort. Gut 63 (2014), 588–597, 10.1136/gutjnl-2013-304636.
Carpenter, H.A., Bacterial and Parasitic Cholangitis, in: Mayo Clinic Proceedings. 1998, Elsevier Ltd, 473–478, 10.1016/S0025-6196(11)63734-8.
Chang, P.V., Hao, L., Offermanns, S., Medzhitov, R., The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 2247–2252, 10.1073/pnas.1322269111.
Chen, Y., Ji, F., Guo, J., Shi, D., Fang, D., Li, L., Dysbiosis of small intestinal microbiota in liver cirrhosis and its association with etiology. Sci. Rep., 6, 2016, 10.1038/srep34055.
Chng, K.R., Chan, S.H., Ng, A.H.Q., Li, C., Jusakul, A., Bertrand, D., Wilm, A., Choo, S.P., Tan, D.M.Y., Lim, K.H., Soetinko, R., Ong, C.K., Duda, D.G., Dima, S., Popescu, I., Wongkham, C., Feng, Z., Yeoh, K.G., Teh, B.T., Yongvanit, P., Wongkham, S., Bhudhisawasdi, V., Khuntikeo, N., Tan, P., Pairojkul, C., Ngeow, J., Nagarajan, N., Tissue microbiome profiling identifies an enrichment of specific enteric bacteria in Opisthorchis viverrini associated cholangiocarcinoma. EBioMedicine 8 (2016), 195–202, 10.1016/j.ebiom.2016.04.034.
Chung, W.S.F., Meijerink, M., Zeuner, B., Holck, J., Louis, P., Meyer, A.S., Wells, J.M., Flint, H.J., Duncan, S.H., Prebiotic potential of pectin and pectic oligosaccharides to promote anti-inflammatory commensal bacteria in the human colon. FEMS Microbiol. Ecol., 93, 2017, 10.1093/femsec/fix127.
Collado, M.C., Donat, E., Ribes-Koninckx, C., Calabuig, M., Sanz, Y., Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease. J. Clin. Pathol. 62 (2009), 264–269, 10.1136/jcp.2008.061366.
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. PLoS One, 8, 2013, e76573, 10.1371/journal.pone.0076573.
Cooper, P.J., Chico, M.E., Rodrigues, L.C., Ordonez, M., Strachan, D., Griffin, G.E., Nutman, T.B., Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics. J. Allergy Clin. Immunol. 111 (2003), 995–1000, 10.1067/mai.2003.1348.
Easton, A.V., Quiñones, M., Vujkovic-Cvijin, I., Oliveira, R.G., Kepha, S., Odiere, M.R., Anderson, R.M., Belkaid, Y., Nutman, T.B., The impact of anthelmintic treatment on human gut microbiota based on cross-sectional and pre- and postdeworming comparisons in Western Kenya. MBio, 10, 2019, 10.1128/mBio.00519-19.
Efimova, D, Tyakht, A, Popenko, A, Vasilyev, A, Altukhov, I, Dovidchenko, N, Odintsova, V, Klimenko, N, Loshkarev, R, Pashkova, M, Elizarova, A, Voroshilova, V, Slavskii, S, Pekov, Y, Filippova, E, Shashkova, T, Levin, E, Alexeev, D, Knomics-Biota a system for exploratory analysis of human gut microbiota data. BioData Min, 11(25), 2018, 10.1186/s13040-018-0187-3.
Elkins, D., Sithithaworn, P., Haswell-Elkins, M., Kaewkes, S., Wongratanacheewin, S., Awacharagan, P., Opisthorchis viverrini: relationships between egg counts, worms recovered and antibody levels within an endemic community in Northeast Thailand. Parasitology 102 (1991), 283–288, 10.1017/S0031182000062600.
Fadrosh, D.W., Ma, B., Gajer, P., Sengamalay, N., Ott, S., Brotman, R.M., Ravel, J., An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 2014, 10.1186/2049-2618-2-6.
Fedorova, O.S., Fedotova, M.M., Sokolova, T.S., Golovach, E.A., Kovshirina, Y.V., Ageeva, T.S., Kovshirina, A.E., Kobyakova, O.S., Ogorodova, L.M., Odermatt, P., Opisthorchis felineus infection prevalence in Western Siberia: a review of Russian literature. Acta Trop., 2018, 10.1016/j.actatropica.2017.11.018.
Fedorova, O.S., Janse, J.J., Ogorodova, L.M., Fedotova, M.M., Achterberg, R.A., Verweij, J.J., Fernández-Rivas, M., Versteeg, S.A., Potts, J., Minelli, C., van Ree, R., Burney, P., Yazdanbakhsh, M., Opisthorchis felineus negatively associates with skin test reactivity in Russia-EuroPrevall-International Cooperation study. Allergy 72 (2017), 1096–1104, 10.1111/all.13120.
Furusawa, Y., Obata, Y., Fukuda, S., Endo, T.A., Nakato, G., Takahashi, D., Nakanishi, Y., Uetake, C., Kato, K., Kato, T., Takahashi, M., Fukuda, N.N., Murakami, S., Miyauchi, E., Hino, S., Atarashi, K., Onawa, S., Fujimura, Y., Lockett, T., Clarke, J.M., Topping, D.L., Tomita, M., Hori, S., Ohara, O., Morita, T., Koseki, H., Kikuchi, J., Honda, K., Hase, K., Ohno, H., Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504 (2013), 446–450, 10.1038/nature12721.
Gauffin Cano, P, Santacruz, A, Moya, A, Sanz, Y, Bacteroides uniformis CECT 7771 ameliorates metabolic and immunological dysfunction in mice with high-fat-diet induced obesity. PLoS One, 7, 2012, 10.1371/journal.pone.0041079.
Gause, W.C., Maizels, R.M., Macrobiota - helminths as active participants and partners of the microbiota in host intestinal homeostasis. Curr. Opin. Microbiol., 2016, 10.1016/j.mib.2016.04.004.
Gophna, U., Sommerfeld, K., Gophna, S., Doolittle, W.F., Veldhuyzen Van Zanten, S.J.O., Differences between tissue-associated intestinal microfloras of patients with Crohn's disease and ulcerative colitis. J. Clin. Microbiol. 44 (2006), 4136–4141, 10.1128/JCM.01004-06.
Gouveia, M.J., Pakharukova, M.Y., Laha, T., Sripa, B., Maksimova, G.A., Rinaldi, G., Brindley, P.J., Mordvinov, V.A., Amaro, T., Santos, L.L., da Costa, J.M.C., Vale, N., Infection with Opisthorchis felineus induces intraepithelial neoplasia of the biliary tract in a rodent model. Carcinogenesis, 2017, 10.1093/carcin/bgx042.
Hiippala, K, Kainulainen, V, Suutarinen, M, Heini, T, Bowers, J R, Jasso-Selles, D, Lemmer, D, Valentine, M, Barnes, R, Engelthaler, D M, Satokari, R, Isolation of anti-inflammatory and epithelium reinforcing Bacteroides and Parabacteroides spp. from a healthy fecal donor. Nutrients, 12, 2020, 10.3390/nu12040935.
Hsieh, Y.-J., Fu, C.-L., Hsieh, M.H., Helminth-induced interleukin-4 abrogates invariant natural killer T cell activation-associated clearance of bacterial infection. Infect. Immun. 82 (2014), 2087–2097, 10.1128/IAI.01578-13.
Ihekweazu, F D, Fofanova, T Y, Queliza, K, Nagy-Szakal, D, Stewart, C J, Engevik, M A, Hulten, K G, Tatevian, N, Graham, D Y, Versalovic, J, Petrosino, J F, Kellermayer, R, Bacteroides ovatus ATCC 8483 monotherapy is superior to traditional fecal transplant and multi-strain bacteriotherapy in a murine colitis model. Gut Microbes 10 (2019), 504–520, 10.1080/19490976.2018.1560753.
Imhann, F., Vila, V., Bonder, A., Fu, M.J., Gevers, J., Visschedijk, D., Spekhorst, M.C., Alberts, L.M., Franke, R., van Dullemen, L., Ter Steege, H.M., Huttenhower, R.W.F., Dijkstra, C., Xavier, G., Festen, R.J., Wijmenga, E.A.M., Zhernakova, C., Weersma, A., R.K., Interplay of host genetics and gut microbiota underlying the onset and clinical presentation of inflammatory bowel disease. Gut 67 (2018), 108–119, 10.1136/gutjnl-2016-312135.
Itthitaetrakool, U., Pinlaor, P., Pinlaor, S., Chomvarin, C., Dangtakot, R., Chaidee, A., Wilailuckana, C., Sangka, A., Lulitanond, A., Yongvanit, P., Chronic Opisthorchis viverrini infection changes the liver microbiome and promotes helicobacter growth. PLoS One, 11, 2016, 10.1371/journal.pone.0165798.
Khokhlova, E.V., Smeianov, V.V., Efimov, B.A., Kafarskaia, L.I., Pavlova, S.I., Shkoporov, A.N., Anti-inflammatory properties of intestinal Bifidobacterium strains isolated from healthy infants. Microbiol. Immunol. 56 (2012), 27–39, 10.1111/j.1348-0421.2011.00398.x.
Klimenko, N.S., Tyakht, A.V., Popenko, A.S., Vasiliev, A.S., Altukhov, I.A., Ischenko, D.S., Shashkova, T.I., Efimova, D.A., Nikogosov, D.A., Osipenko, D.A., Musienko, S.V, Selezneva, K.S., Baranova, A., Kurilshikov, A.M., Toshchakov, S.M., Korzhenkov, A.A., Samarov, N.I., Shevchenko, M.A., Tepliuk, A.V, Alexeev, D.G., Microbiome responses to an uncontrolled short-term diet intervention in the frame of the citizen science project. Nutrients, 10, 2018, 10.3390/nu10050576.
Kumari, R., Ahuja, V., Paul, J., Fluctuations in butyrate-producing bacteria in ulcerative colitis patients of North India. World J. Gastroenterol. 19 (2013), 3404–3414, 10.3748/wjg.v19.i22.3404.
Kuznetsova, A., Brockhoff, P.B., Christensen, R.H.B., lmerTest package: tests in linear mixed effects models. J. Stat. Softw., 82, 2017, 10.18637/jss.v082.i13.
Lai, C.K.W., Beasley, R., Crane, J., Foliaki, S., Shah, J., Weiland, S., Aït-Khaled, N., Anderson, H.R., Asher, M.I., Beasley, R., Björksten, B., Brunekreef, B., Crane, J., Ellwood, P., Flohr, C., Foliaki, S., Forastiere, F., García-Marcos, L., Keil, U., Lai, C.K.W., Mallol, J., Mitchell, E.A., Montefort, S., Odhiambo, J., Pearce, N., Robertson, C.F., Shah, J., Stewart, A.W., Strachan, D., Von Mutius, E., Weiland, S.K., Weinmayr, G., Williams, H., Wong, G., Global variation in the prevalence and severity of asthma symptoms: phase three of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax 64 (2009), 476–483, 10.1136/thx.2008.106609.
Lenth, R., emmeans: Estimated Marginal Means, aka Least-Squares Means. 2019.
Liu, J., Wu, D., Ahmed, A., Li, X., Ma, Y., Tang, L., Mo, D., Ma, Y., Xin, Y., Comparison of the gut microbe profiles and numbers between patients with liver cirrhosis and healthy individuals. Curr. Microbiol. 65 (2012), 7–13, 10.1007/s00284-012-0105-8.
Louis, P., Flint, H.J., Diversity, Metabolism and Microbial Ecology of Butyrate-Producing Bacteria from the Human Large Intestine. 2009, 10.1111/j.1574-6968.2009.01514.x.
Lu, H., Wu, Z., Xu, W., Yang, J., Chen, Y., Li, L., Intestinal microbiota was assessed in cirrhotic patients with hepatitis B virus infection. Intestinal microbiota of HBV cirrhotic patients. Microb. Ecol. 61 (2011), 693–703, 10.1007/s00248-010-9801-8.
Lv, L.X., Fang, D.Q., Shi, D., Chen, D.Y., Yan, R., Zhu, Y.X., Chen, Y.F., Shao, L., Guo, F.F., Wu, W.R., Li, A., Shi, H.Y., Jiang, X.W., Jiang, H.Y., Xiao, Y.H., Zheng, S.S., Li, L.J., Alterations and correlations of the gut microbiome, metabolism and immunity in patients with primary biliary cirrhosis. Environ. Microbiol. 18 (2016), 2272–2286, 10.1111/1462-2920.13401.
Machiels, K., Joossens, M., Sabino, J., De Preter, V., Arijs, I., Eeckhaut, V., Ballet, V., Claes, K., Van Immerseel, F., Verbeke, K., Ferrante, M., Verhaegen, J., Rutgeerts, P., Vermeire, S., A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 63 (2014), 1275–1283, 10.1136/gutjnl-2013-304833.
Maizels, R.M., McSorley, H.J., Regulation of the host immune system by helminth parasites. J. Allergy Clin. Immunol. 138 (2016), 666–675, 10.1016/j.jaci.2016.07.007.
Maizels, R.M., Smits, H.H., McSorley, H.J., Modulation of host immunity by Helminths: the expanding repertoire of parasite effector molecules. Immunity 49 (2018), 801–818, 10.1016/j.immuni.2018.10.016.
Martino, C., Morton, J.T., Marotz, C.A., Thompson, L.R., Tripathi, A., Knight, R., Zengler, K., A novel sparse compositional technique reveals microbial perturbations. mSystems, 4, 2019, 10.1128/msystems.00016-19.
McCracken, B.A., Nathalia Garcia, M., Phylum Synergistetes in the oral cavity: a possible contributor to periodontal disease. Anaerobe, 2020, 10.1016/j.anaerobe.2020.102250.
McDonald, D., Hyde, E., Debelius, J.W., Morton, J.T., Gonzalez, A., Ackermann, G., Aksenov, A.A., Behsaz, B., Brennan, C., Chen, Y., De Right Goldasich, L., Dorrestein, P.C., Dunn, R.R., Fahimipour, A.K., Gaffney, J., Gilbert, J.A., Gogul, G., Green, J.L., Hugenholtz, P., Humphrey, G., Huttenhower, C., Jackson, M.A., Janssen, S., Jeste, D.V., Jiang, L., Kelley, S.T., Knights, D., Kosciolek, T., Ladau, J., Leach, J., Marotz, C., Meleshko, D., Melnik, A.V., Metcalf, J.L., Mohimani, H., Montassier, E., Navas-Molina, J., Nguyen, T.T., Peddada, S., Pevzner, P., Pollard, K.S., Rahnavard, G., Robbins-Pianka, A., Sangwan, N., Shorenstein, J., Smarr, L., Song, S.J., Spector, T., Swafford, A.D., Thackray, V.G., Thompson, L.R., Tripathi, A., Vázquez-Baeza, Y., Vrbanac, A., Wischmeyer, P., Wolfe, E., Zhu, Q., Knight, R., Mann, A.E., Amir, A., Frazier, A., Martino, C., Lebrilla, C., Lozupone, C., Lewis, C.M., Raison, C., Zhang, C., Lauber, C.L., Warinner, C., Lowry, C.A., Callewaert, C., Bloss, C., Willner, D., Galzerani, D.D., Gonzalez, D.J., Mills, D.A., Chopra, D., Gevers, D., Berg-Lyons, D., Sears, D.D., Wendel, D., Lovelace, E., Pierce, E., TerAvest, E., Bolyen, E., Bushman, F.D., Wu, G.D., Church, G.M., Saxe, G., Holscher, H.D., Ugrina, I., German, J.B., Caporaso, J.G., Wozniak, J.M., Kerr, J., Ravel, J., Lewis, J.D., Suchodolski, J.S., Jansson, J.K., Hampton-Marcell, J.T., Bobe, J., Raes, J., Chase, J.H., Eisen, J.A., Monk, J., Clemente, J.C., Petrosino, J., Goodrich, J., Gauglitz, J., Jacobs, J., Zengler, K., Swanson, K.S., Lewis, K., Mayer, K., Bittinger, K., Dillon, L., Zaramela, L.S., Schriml, L.M., Dominguez-Bello, M.G., Jankowska, M.M., Blaser, M., Pirrung, M., Minson, M., Kurisu, M., Ajami, N., Gottel, N.R., Chia, N., Fierer, N., White, O., Cani, P.D., Gajer, P., Strandwitz, P., Kashyap, P., Dutton, R., Park, R.S., Xavier, R.J., Mills, R.H., Krajmalnik-Brown, R., Ley, R., Owens, S.M., Klemmer, S., Matamoros, S., Mirarab, S., Moorman, S., Holmes, S., Schwartz, T., Eshoo-Anton, T.W., Vigers, T., Pandey, V., Treuren, W.V., Fang, X., Xu, Z., Jarmusch, Z., Geier, A., Reeve, J., Silva, N., Kopylova, R., Nguyen, E., Sanders, D., Salido Benitez, K., Heale, R.A., Abramson, A.C., Waldispühl, M., Butyaev, J., Drogaris, A., Nazarova, C., Ball, E., Gunderson, M., B., American gut: an open platform for citizen science microbiome research. mSystems, 3, 2018, 10.1128/msystems.00031-18.
McMurdie, P.J., Holmes, S., Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8, 2013, 10.1371/journal.pone.0061217.
Mondot, S., Kang, S., Furet, J.P., Aguirre de Carcer, D., McSweeney, C., Morrison, M., Marteau, P., Doré, J., Leclerc, M., Highlighting new phylogenetic specificities of Crohnʼs disease microbiota. Inflamm. Bowel Dis. 17 (2011), 185–192, 10.1002/ibd.21436.
Morgan, X.C., Tickle, T.L., Sokol, H., Gevers, D., Devaney, K.L., Ward, D.V., Reyes, J.A., Shah, S.A., LeLeiko, N., Snapper, S.B., Bousvaros, A., Korzenik, J., Sands, B.E., Xavier, R.J., Huttenhower, C., Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol., 13, 2012, R79, 10.1186/gb-2012-13-9-r79.
Nadal, I., Donant, E., Ribes-Koninckx, C., Calabuig, M., Sanz, Y., Sanz, Y., Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J. Med. Microbiol. 56 (2007), 1669–1674, 10.1099/jmm.0.47410-0.
Nishida, A., Inoue, R., Inatomi, O., Bamba, S., Naito, Y., Andoh, A., Gut microbiota in the pathogenesis of inflammatory bowel disease. Clin. J. Gastroenterol. 11 (2018), 1–10, 10.1007/s12328-017-0813-5.
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E., Wagner, H., 2019. vegan: Community ecology package.
Ohkusa, T, Yoshida, T, Sato, N, Watanabe, S, Tajiri, H, Okayasu, I, Commensal bacteria can enter colonic epithelial cells and induce proinflammatory cytokine secretion: A possible pathogenic mechanism of ulcerative colitis. J. Med. Microbiol 58 (2009), 535–545, 10.1099/jmm.0.005801-0.
Park, J., Kim, M., Kang, S.G., Jannasch, A.H., Cooper, B., Patterson, J., Kim, C.H., Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR-S6K pathway. Mucosal Immunol. 8 (2015), 80–93, 10.1038/mi.2014.44.
Park, S.K., Kim, M.S., Roh, S.W., Bae, J.W., Blautia stercoris sp. nov., isolated from human faeces. Int. J. Syst. Evol. Microbiol. 62 (2012), 776–779, 10.1099/ijs.0.031625-0.
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. FASEB J. 27 (2013), 4572–4584, 10.1096/fj.13-232751.
R Core Team. R: A Language and Environment for Statistical Computing. 2019.
Ramanan, D., Bowcutt, R., Lee, S.C., Tang, M.S., Kurtz, Z.D., Ding, Y., Honda, K., Gause, W.C., Blaser, M.J., Bonneau, R.A., Lim, Y.A.L., Loke, P., Cadwell, K., Helminth infection promotes colonization resistance via type 2 immunity. Science 352 (2016), 608–612, 10.1126/science.aaf3229.
Renaud, G., Stenzel, U., Maricic, T., Wiebe, V., Kelso, J., DeML: robust demultiplexing of Illumina sequences using a likelihood-based approach. Bioinformatics 31 (2015), 770–772, 10.1093/bioinformatics/btu719.
Repass, J., Maherali, N., Owen, K., Reproducibility Project: Cancer Biology, R.P.C., Reproducibility Project Cancer Biology. Registered report: Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Elife, 5, 2016, 10.7554/eLife.10012.
Reynolds, L.A., Redpath, S.A., Yurist-Doutsch, S., Gill, N., Brown, E.M., van der Heijden, J., Brosschot, T.P., Han, J., Marshall, N.C., Woodward, S.E., Valdez, Y., Borchers, C.H., Perona-Wright, G., Finlay, B.B., Enteric helminths promote salmonella coinfection by altering the intestinal metabolome. J. Infect. Dis. 215 (2017), 1245–1254, 10.1093/infdis/jix141.
Reynolds, L.A., Smith, K.A., Filbey, K.J., Harcus, Y., Hewitson, J.P., Redpath, S.A., Valdez, Y., Yebra, M.J., Finlay, B.B., Maizels, R.M., Commensal-pathogen interactions in the intestinal tract: lactobacilli promote infection with, and are promoted by, helminth parasites. Gut Microbes 5 (2014), 522–532, 10.4161/gmic.32155.
Rosa, B.A., Supali, T., Gankpala, L., Djuardi, Y., Sartono, E., Zhou, Y., Fischer, K., Martin, J., Tyagi, R., Bolay, F.K., Fischer, P.U., Yazdanbakhsh, M., Mitreva, M., Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia. Microbiome, 6, 2018, 10.1186/s40168-018-0416-5.
Saltykova, I.V., Petrov, V.A., Dorofeeva, Y.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. Immanuel Kant Balt. Fed. Univ., 2017, 70–78.
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. PLoS Negl. Trop. Dis., 10, 2016, e0004809, 10.1371/journal.pntd.0004809.
Sanduzzi Zamparelli, M., Rocco, A., Compare, D., Nardone, G., The gut microbiota: a new potential driving force in liver cirrhosis and hepatocellular carcinoma. United Eur. Gastroenterol. J. 5 (2017), 944–953, 10.1177/2050640617705576.
Schachter, J., De Oliveira, D.A., Da Silva, C.M., De Barros Alencar, A.C.M., Duarte, M., Da Silva, M.M.P., De Paula Rosa Ignácio, A.C., Lopes-Torres, E.J., Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation. Infect. Immun., 88, 2020, 10.1128/IAI.00642-19.
Scholte, L.L.S., Pascoal-Xavier, M.A., Nahum, L.A., Helminths and cancers from the evolutionary perspective. Front. Med., 2018, 10.3389/fmed.2018.00090.
Sripa, B., Thinkhamrop, B., Mairiang, E., Laha, T., Kaewkes, S., Sithithaworn, P., Periago, M.V., Bhudhisawasdi, V., Yonglitthipagon, P., Mulvenna, J., Brindley, P.J., Loukas, A., Bethony, J.M., Elevated plasma IL-6 associates with increased risk of advanced fibrosis and cholangiocarcinoma in individuals infected by opisthorchis viverrini. PLoS Negl. Trop. Dis., 6, 2012, 10.1371/journal.pntd.0001654.
Su, C., Su, L., Li, Y., Long, S.R., Chang, J., Zhang, W., Walker, W.A., Xavier, R.J., Cherayil, B.J., Shi, H.N., Helminth-induced alterations of the gut microbiota exacerbate bacterial colitis. Mucosal Immunol. 11 (2018), 144–157, 10.1038/mi.2017.20.
Swidsinski, A., Ladhoff, A., Pernthaler, A., Swidsinski, S., Loening-Baucke, V., Ortner, M., Weber, J., Hoffmann, U., Schreiber, S., Dietel, M., Lochs, H., Mucosal flora in inflammatory bowel disease. Gastroenterology 122 (2002), 44–54, 10.1053/gast.2002.30294.
Takahashi, K., Nishida, A., Fujimoto, T., Fujii, M., Shioya, M., Imaeda, H., Inatomi, O., Bamba, S., Andoh, A., Sugimoto, M., Reduced abundance of butyrate-producing bacteria species in the fecal microbial community in Crohn's disease. Digestion 93 (2016), 59–65, 10.1159/000441768.
Therneau, T.M., n.d. Survival Analysis [R package survival version 2.44-1.1].
Tremblay, J., Singh, K., Fern, A., Kirton, E.S., He, S., Woyke, T., Lee, J., Chen, F., Dangl, J.L., Tringe, S.G., Primer and platform effects on 16S rRNA tag sequencing. Front. Microbiol., 6, 2015, 771, 10.3389/fmicb.2015.00771.
Tyakht, A.V., Manolov, A.I., Kanygina, A.V., Ischenko, D.S., Kovarsky, B.A., Popenko, A.S., Pavlenko, A.V., Elizarova, A.V., Rakitina, D.V., Baikova, J.P., Ladygina, V.G., Kostryukova, E.S., Karpova, I.Y., Semashko, T.A., Larin, A.K., Grigoryeva, T.V., Sinyagina, M.N., Malanin, S.Y., Shcherbakov, P.L., Kharitonova, A.Y., Khalif, I.L., Shapina, M.V., Maev, I.V., Andreev, D.N., Belousova, E.A., Buzunova, Y.M., Alexeev, D.G., Govorun, V.M., Genetic diversity of Escherichia coli in gut microbiota of patients with Crohn's disease discovered using metagenomic and genomic analyses. BMC Genomics, 19, 2018, 968, 10.1186/s12864-018-5306-5.
Varela, E., Manichanh, C., Gallart, M., Torrejón, A., Borruel, N., Casellas, F., Guarner, F., Antolin, M., Colonisation by Faecalibacterium prausnitzii and maintenance of clinical remission in patients with ulcerative colitis. Aliment. Pharmacol. Ther. 38 (2013), 151–161, 10.1111/apt.12365.
Venables, W.N., Ripley, B.D., MASS package. Modern Applied Statistics with S, 2002, Springer.
Verhoog, S., Taneri, P.E., Díaz, Z.M.R., Marques-Vidal, P., Troup, J.P., Bally, L., Franco, O.H., Glisic, M., Muka, T., Dietary factors and modulation of bacteria strains of akkermansia muciniphila and faecalibacterium prausnitzii: a systematic review. Nutrients, 2019, 10.3390/nu11071565.
Walk, S.T., Blum, A.M., Ewing, S.A.-S., Weinstock, J.V., Young, V.B., Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus. Inflamm. Bowel Dis. 16 (2010), 1841–1849, 10.1002/ibd.21299.
Wammes, L.J., Hamid, F., Wiria, A.E., May, L., Kaisar, M.M.M., Prasetyani-Gieseler, M.A., Djuardi, Y., Wibowo, H., Kruize, Y.C.M., Verweij, J.J., de Jong, S.E., Tsonaka, R., Houwing-Duistermaat, J.J., Sartono, E., Luty, A.J.F., Supali, T., Yazdanbakhsh, M., Community deworming alleviates geohelminth-induced immune hyporesponsiveness. Proc. Natl. Acad. Sci. 113 (2016), 12526–12531, 10.1073/pnas.1604570113.
Wei, Y., Li, Yanmei, Yan, L., Sun, C., Miao, Q., Wang, Q., Xiao, X., Lian, M., Li, B., Chen, Y., Zhang, J., Li, You, Huang, B., Li, Yikang, Cao, Q., Fan, Z., Chen, X., Fang, J.Y., Gershwin, M.E., Tang, R., Ma, X., Alterations of gut microbiome in autoimmune hepatitis. Gut 69 (2020), 569–577, 10.1136/gutjnl-2018-317836.
Wendel-Haga, M., Celius, E.G., Is the hygiene hypothesis relevant for the risk of multiple sclerosis?. Acta Neurol. Scand. 136 (2017), 26–30, 10.1111/ane.12844.
Wickham, H., Sci. Am. 272:3 (2006), 82–88 35, 2006.
Xu, M., Jiang, Z., Huang, W., Yin, J., Ou, S., Jiang, Y., Meng, L., Cao, S., Yu, A., Cao, J., Shen, Y., Altered gut microbiota composition in subjects infected with Clonorchis sinensis. Front. Microbiol., 9, 2018, 10.3389/fmicb.2018.02292.
Yazdanbakhsh, M., van den Biggelaar, A., Maizels, R.M., Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol. 22 (2001), 372–377.
Yilmaz, P., Parfrey, L.W., Yarza, P., Gerken, J., Pruesse, E., Quast, C., Schweer, T., Peplies, J., Ludwig, W., Glöckner, F.O., The SILVA and “all-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res., 42, 2014, 10.1093/nar/gkt1209 D643.
Zaiss, M.M., Rapin, A., Lebon, L., Dubey, L.K., Mosconi, I., Sarter, K., Piersigilli, A., Menin, L., Walker, A.W., Rougemont, J., Paerewijck, O., Geldhof, P., McCoy, K.D., Macpherson, A.J., Croese, J., Giacomin, P.R., Loukas, A., Junt, T., Marsland, B.J., Harris, N.L., The intestinal microbiota contributes to the ability of helminths to modulate allergic inflammation. Immunity, 43, 2015, 998, 10.1016/J.IMMUNI.2015.09.012.
Zhang, C, Zhang, M, Wang, S, Han, R, Cao, Y, Hua, W, Mao, Y, Zhang, X, Pang, X, Wei, C, Zhao, G, Chen, Y, Zhao, L, Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J 4 (2010), 232–241, 10.1038/ismej.2009.112.
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. Crit. Public Health 28 (2018), 534–545, 10.1080/09581596.2017.1378425.