Relationships Between Gastrointestinal Parasite Infections and the Fecal Microbiome in Free-Ranging Western Lowland Gorillas

. 2018 ; 9 () : 1202. [epub] 20180615

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid29963018

Relationships between gastrointestinal parasites (GIPs) and the gastrointestinal microbiome (GIM) are widely discussed topics across mammalian species due to their possible impact on the host's health. GIPs may change the environment determining alterations in GIM composition. We evaluated the associations between GIP infections and fecal microbiome composition in two habituated and two unhabituated groups of wild western lowland gorillas (Gorilla g. gorilla) from Dzanga Sangha Protected Areas, Central African Republic. We examined 43 fecal samples for GIPs and quantified strongylid nematodes. We characterized fecal microbiome composition through 454 pyrosequencing of the V1-V3 region of the bacterial 16S rRNA gene. Entamoeba spp. infections were associated with significant differences in abundances of bacterial taxa that likely play important roles in nutrition and metabolism for the host, besides being characteristic members of the gorilla gut microbiome. We did not observe any relationships between relative abundances of several bacterial taxa and strongylid egg counts. Based on our findings, we suggest that there is a significant relationship between fecal microbiome and Entamoeba infection in wild gorillas. This study contributes to the overall knowledge about factors involved in modulating GIM communities in great apes.

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Anderson R. M., Schad G. A. (1985). Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Trans. R. Soc. Trop. Med. Hyg. 79, 812–825. 10.1016/0035-9203(85)90128-2 PubMed DOI

Audebert C., Even G., Cian A., Loywick A., Merlin S., et al. . (2016). Colonization with the enteric protozoa Blastocystis is associated with increased diversity of human gut bacterial microbiota. Sci. Rep. 6:25255. 10.1038/srep25255 PubMed DOI PMC

Berg R. (1996). The indigenous gastrointestinal microflora. Trends Microbiol. 4, 430–435. 10.1016/0966-842X(96)10057-3 PubMed DOI

Berrilli F., Di Cave D., Cavallero S., D'Amelio S. (2012). Interactions between parasites and microbial communities in the human gut. Front. Cell. Infect. Microbiol. 2:141. 10.3389/fcimb.2012.00141 PubMed DOI PMC

Bracha R., Kobiler D., Mirelman D. (1982). Attachment and ingestion of bacteria by trophozoites of Entamoeba histolytica. Infect. Immun. 36, 396–406. PubMed PMC

Buffie C. G., Pamer E. G. (2013). Microbiota-mediated colonization resistance against intestinal pathogens. Nat. Rev. Immunol. 13, 790–801. 10.1038/nri3535 PubMed DOI PMC

Burgess S. L., Petri W. A., Jr. (2016). The intestinal bacterial microbiome and E. histolytica infection. Curr. Trop. Med. Rep. 3, 71–74. 10.1007/s40475-016-0083-1 PubMed DOI PMC

Burgunder J., Pafčo B., Petrželková K. J., Modrý D., Hashimoto C., MacIntosh A. J. J. (2017). Complexity in behavioural organization and strongylid infection among wild chimpanzees. Anim. Behav. 129, 257–268. 10.1016/j.anbehav.2017.06.002 DOI

Bush A. O., Lafferty K. D., Lotz J. M., Shostak A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83, 575–583. 10.2307/3284227 PubMed DOI

Cabaret J., Gasnier N., Jacquiet P. (1998). Faecal egg counts are representative of digestive-tract strongyle worm burdens in sheep and goats. Parasite 5, 137–142. 10.1051/parasite/1998052137 PubMed DOI

Cantacessi C., Giacomin P., Croese J., Zakrzewski M., Sotillo J., McCann L., et al. . (2014). Impact of experimental hookworm infection on the human gut microbiota. J. Infect. Dis. 210, 1431–1434. 10.1093/infdis/jiu256 PubMed DOI PMC

Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., et al. . (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336. 10.1038/nmeth.f.303 PubMed DOI PMC

Červená B., Vallo P., Pafčo B., Jirku K., Jirku M., Petrželková K. J., et al. . (2017). Host specificity and basic ecology of Mammomonogamus (Nematoda, Syngamidae) from lowland gorillas and forest elephants in Central African Republic. Parasitology 144, 1016–1025. 10.1017/S0031182017000221 PubMed DOI

Chapman C. A., Speirs M. L., Gillespie T. R., Holland T., Austad K. M. (2006). Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups. Am. J. Primatol. 68, 397–409. 10.1002/ajp.20233 PubMed DOI

Consortium T. H. M. P. (2012). Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214. 10.1038/nature11234 PubMed DOI PMC

Cooper P., Walker A. W., Reyes J., Chico M., Salter S. J., Vaca M., et al. . (2013). Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota. PLoS ONE 8:e76573. 10.1371/journal.pone.0076573 PubMed DOI PMC

Cox F. E. (2002). History of human parasitology. Clin. Microbiol. Rev. 15, 595–612. 10.1128/CMR.15.4.595-612.2002 PubMed DOI PMC

Daveson A. J., Jones D. M., Gaze S., McSorley H., Clouston A., Pascoe A., et al. . (2011). Effect of hookworm infection on wheat challenge in celiac disease - a randomised double-blinded placebo controlled trial. PLoS ONE 6:e17366. 10.1371/journal.pone.0017366 PubMed DOI PMC

Dufrêne M., Legendre P. (1997). Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67, 345–366. 10.2307/2963459 DOI

Eckburg P. B., Bik E. M., Bernstein C. N., Purdom E., Dethlefsen L., Sargent M., et al. . (2005). Diversity of the human intestinal microbial flora. Science 308, 1635 –1638. 10.1126/science.1110591 PubMed DOI PMC

Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200. 10.1093/bioinformatics/btr381 PubMed DOI PMC

Elliott D. E., Summers R. W., Weinstock J. V. (2007). Helminths as governors of immune-mediated inflammation. Int. J. Parasitol. 37, 457–464. 10.1016/j.ijpara.2006.12.009 PubMed DOI

Gálván-Moroyoqui J. M., Del Carmen Domínguez-Robles M., Franco E., Meza I. (2008). The Interplay between Entamoeba and enteropathogenic bacteria modulates epithelial cell damage. PLoS Negl. Trop. Dis. 2:e266. 10.1371/journal.pntd.0000266 PubMed DOI PMC

Gomez A., Petrzelkova K., Yeoman C. J., Vlckova K., Mrázek J., Koppova I., et al. . (2015). Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology. Mol. Ecol. 24, 2551–2565. 10.1111/mec.13181 PubMed DOI

Gomez A., Petrzelkova K. J., Burns M. B., Yeoman C. J., Amato K. R., Vlckova K., et al. . (2016a). Gut microbiome of coexisting BaAka pygmies and Bantu reflects gradients of traditional subsistence patterns. Cell Rep. 14, 2142–2153. 10.1016/j.celrep.2016.02.013 PubMed DOI

Gomez A., Rothman J. M., Petrzelkova K., Yeoman C. J., Vlckova K., Umaña J. D., et al. . (2016b). Temporal variation selects for diet-microbe co-metabolic traits in the gut of Gorilla spp. ISME J. 10, 514–526. 10.1038/ismej.2015.146 PubMed DOI PMC

González-Hernández M., Rangel-Negrín A., Schoof V. A. M., Chapman C. A., Canales-Espinosa D., Dias P. A. D. (2014). Transmission patterns of pinworms in two sympatric congeneric primate species. Int. J. Primatol. 35, 445–462. 10.1007/s10764-014-9751-y DOI

Guinane C. M., Cotter P. D. (2013). Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ. Ther. Adv. Gastroenterol. 6, 295–308. 10.1177/1756283X13482996 PubMed DOI PMC

Hasegawa H., Modrý D., Kitagawa M., Shutt K. A., Todd A., Kalousová B., et al. . (2014). Humans and great apes cohabiting the forest ecosystem in central African Republic Harbour the same hookworms. PLoS Negl. Trop. Dis. 8:e2715. 10.1371/journal.pntd.0002715 PubMed DOI PMC

Hayes K. S., Bancroft A. J., Goldrick M., Portsmouth C., Roberts I. S., Grencis R. K. (2010). Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science 328, 1391–1394. 10.1126/science.1187703 PubMed DOI PMC

Hiemstra H., Klaver E., Vrijland K., Kringel H., Andreasen A., Bouma G., et al. . (2014). Excreted/secreted Trichuris suis products reduce barrier function andsuppress inflammatory cytokine production of intestinalepithelial cells. Mol. Immunol. 60, 1–7. 10.1016/j.molimm.2014.03.003 PubMed DOI

Hodges M., Koroma M. M., Baldé M. S., Turay H., Fofanah I., Divall M. J., et al. . (2011). Current status of schistosomiasis and soil-transmitted helminthiasis in Beyla and Macenta Prefectures, Forest Guinea. Trans. R. Soc. Trop. Med. Hyg. 105, 672–674. 10.1016/j.trstmh.2011.07.008 PubMed DOI

Isolauri E., Salminen S., Ouwehand A. C. (2004). Probiotics. Best Pract. Res. Clin. Gastroenterol. 18, 299–313. 10.1016/j.bpg.2003.10.006 PubMed DOI

Kaakoush N. O. (2015). Insights into the role of Erysipelotrichaceae in the human host. Front. Cell Infect. Microbiol. 5:84. 10.3389/fcimb.2015.00084 PubMed DOI PMC

Kalousová B. (2013). Gastrointestinal parasites of Wild Western Lowland Gorillas (Gorilla gorilla gorilla) in Dzanga Sector of Dzanga-Ndoki National Park, Central African Republic. Master thesis. Masaryk University. Czechia.

Kalousová B. (2015). Parasites of gorillas, in Parasites of Great Apes: Atlas of Coproscopic Diagnostics, eds Modrý D., Petrželková K., Kalousová B., Hasegawa H. (Brno: HPI-lab, University of Veterinary and Pharm. Sciences Brno, Czech Republic; ), 103–106.

Kalousová B., Hasegawa H., Petrželková K. J., Sakamaki T., Kooriyma T., Modrý D. (2016). Adult hookworms (Necator spp.) collected from researchers working with wild western lowland gorillas. Parasit. Vectors 9:75. 10.1186/s13071-016-1357-0 PubMed DOI PMC

Kassai T. (1999). Veterinary Helminthology, 1st Edn. Oxford: Butterworth Heinmann Ltd.

Koike S., Yoshitani S., Kobayashi Y., Tanaka K. (2003). Phylogenetic analysis of fiber-associated rumen bacterial community and PCR detection of uncultured bacteria. FEMS Microbiol. Lett. 229, 23–30. 10.1016/S0378-1097(03)00760-2 PubMed DOI

Kreisinger J., Bastien G., Hauffe H. C., Marchesi J., Perkins S. E. (2015). Interactions between multiple helminths and the gut microbiota in wild rodents. Philos. Trans. R. Soc. B 370:20140295 10.1098/rstb.2014.0295 PubMed DOI PMC

Kumar S., Filipski A., Swarna V., Walker A., Hedges S. B. (2005). Placing confidence limits on the molecular age of the human-chimpanzee divergence. Proc. Natl. Acad. Sci. U.S.A. 102, 18842–18847. 10.1073/pnas.0509585102 PubMed DOI PMC

Landsoud-Soukate J., Tutin C. E., Fernandez M. (1995). Intestinal parasites of sympatric gorillas and chimpanzees in the Lopé Reserve, Gabon. Ann. Trop. Med. Parasit. 89 73–79. 10.1080/00034983.1995.11812931 PubMed DOI

Lay C., Sutren M., Rochet V., Saunier K., Doré J., Rigottier-Gois L. (2005). Design and validation of 16S rRNA probes to enumerate members of the Clostridium leptum subgroup in human faecal microbiota. Environ. Microbiol. 7, 933–946. 10.1111/j.1462-2920.2005.00763.x PubMed DOI

Liaw A., Wiener M. (2002). Classification and regression by randomforest. R News 2, 18–22.

Lilly A. A., Mehlman P. T., Doran D. (2002). Intestinal parasites in gorillas, chimpanzees, and humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. Int. J. Primatol. 23, 555–573. 10.1023/A:1014969617036 DOI

Mackie R. I., Sghir A., Gaskins H. R. (1999). Developmental microbial ecology of the neonatal gastrointestinal tract. Am. J. Clin. Nutr. 69, 1035–1045. 10.1093/ajcn/69.5.1035s PubMed DOI

Masi S., Chauffour S., Bain O., Todd A., Guillot J., Krief S. (2012). Seasonal effects on great ape health: a case study of wild chimpanzees and western gorillas. PLoS ONE 7:e49805. 10.1371/journal.pone.0049805 PubMed DOI PMC

Mekonnen Z., Levecke B., Boulet G., Bogers J.-P., Vercruysse J. (2013). Efficacy of different albendazole and mebendazole regimens against heavy-intensity Trichuris trichiura infections in school children, Jimma Town, Ethiopia. Pathog. Glob. Health 107, 207–209. 10.1179/2047773213Y.0000000092 PubMed DOI PMC

Moeller A. H., Foerster S., Wilson M. L., Pusey A. E., Hahn B. H., Ochman H. (2016). Social behavior shapes the chimpanzee pan-microbiome. Sci. Adv. 2:e1500997. 10.1126/sciadv.1500997 PubMed DOI PMC

Moeller A. H., Li Y., Mpoudi Ngole E., Ahuka-Mundeke S., Lonsdorf E. V., Pusey A. E., et al. . (2014). Rapid changes in the gut microbiome during human evolution. Proc. Natl. Acad. Sci. U.S.A. 111, 16431–16435. 10.1073/pnas.1419136111 PubMed DOI PMC

Moeller A. H., Peeters M., Ayouba A., Ngole E. M., Esteban A., Hahn B. H., et al. . (2015). Stability of the gorilla microbiome despite simian immunodeficiency virus infection. Mol. Ecol. 24, 690–697. 10.1111/mec.13057 PubMed DOI PMC

Mohammadi R., Hosseini-Safa A., Ehsani Ardakani M. J., Rostami-Nejad M. (2015). The relationship between intestinal parasites and some immune-mediated intestinal conditions. Gastroenterol. Hepatol. Bed Bench 8, 123–131. PubMed PMC

Moreels T. G., Pelckmans P. A. (2005). Gastrointestinal parasites. Potential therapy for refractory inflammatory bowel diseases. Inflamm. Bowel Dis. 11, 178–184. 10.1097/00054725-200502000-00012 PubMed DOI

Morton E. R., Lynch J., Froment A., Lafosse S., Heyer E., Przeworski M., et al. . (2015). Variation in rural African gut microbiomes is strongly shaped by parasitism and diet. PLoS Genet. 11:e1005658. 10.1371/journal.pgen.1005658 PubMed DOI PMC

Müller-Graf C., Collins D., Woolhouse M. E. (1996). Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 112, 489–497. 10.1017/S0031182000076952 PubMed DOI

Ngobeni R., Samie A., Moonah S., Watanabe K., Petri W. A., Jr, Gilchrist C. (2017). Entamoeba species in South Africa: correlations with the host microbiome, parasite burdens, and first description of Entamoeba bangladeshi outside of asia. J. Infect. Dis. 216, 1592–1600. 10.1093/infdis/jix535 PubMed DOI PMC

Nielsen M., Pfisterb K., von Samson-Himmelstjerna G. (2014). Selective therapy in equine parasite control-application and limitations. Vet. Parasitol. 202, 95–103. 10.1016/j.vetpar.2014.03.020 PubMed DOI

Obregon-Tito A. J., Tito R. Y., Metcalf J., Sankaranarayanan K., Clemente J. C., Ursell L. K., et al. . (2015). Subsistence strategies in traditional societies distinguish gut microbiomes. Nat. Commun. 6:6505. 10.1038/ncomms7505 PubMed DOI PMC

Ochman H., Worobey M., Kuo C.-H., Ndjango J.-B. N., Peeters M., Hahn B. H., et al. . (2010). Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 8:e1000546. 10.1371/journal.pbio.1000546 PubMed DOI PMC

Oksanen J., Blanchet F. G., Kindt R., Legendre P., Minchin P. R., O'Hara R. B., et al. (2013). Vegan: Community Ecology Package. R package version 2.0-10.

Pafčo B., Benavides J. A., Pšenková-Profousová I., Modrý D., Červená B., Shutt K. A., et al. . (2017). Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas? Parasitol. Res. 116, 3401–3410. 10.1007/s00436-017-5667-8 PubMed DOI

Pafčo B., Čížkovaá D., Kreisinger J., Hasegawa H., Vallo P., Shutt K., et al. . (2018). Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Sci. Rep. 8:5933. 10.1038/s41598-018-24126-3 PubMed DOI PMC

Piekarska J., Płoneczka-Janeczko K., Kantyka M., Kuczaj M., Gorczykowski M., Janeczko K. (2013). Gastrointestinal nematodes in grazing dairy cattle from small and medium-sized farms in southern Poland. Vet. Parasitol. 198, 250–253. 10.1016/j.vetpar.2013.07.039 PubMed DOI

R Development Core Team (2008). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.

Rani R., Murthy R. S., Bhattacharya S., Ahuja V., Rizvi M. A., Paul J. (2006). Changes in bacterial profile during amebiasis: demonstration of anaerobic bacteria in ALA pus samples. Am. J. Trop. Med. Hyg. 75, 880–885. PubMed

Reddy M. V. (2010). Immunomodulators of helminthes: promising therapeutics for autoimmune disorders and allergic diseases x. Indian J. Clin. Biochem. 25, 109–110. 10.1007/s12291-010-0021-2 PubMed DOI PMC

Revelle W. (2017). psych: Procedures for Psychological, Psychometric, and Personality Research. R package version 1.7.5. Evanston, IL: Northwestern University.

Roberts D. W. (2013). Labdsv: Ordination and Multivariate Analysis for Ecology. R package version 1.6-1.

Rosa B. A., Supali T., Gankpala L., Djuardi Y., Sartono E., Zhou Y., et al. . (2018). Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia. Microbiome 6:33. 10.1186/s40168-018-0416-5 PubMed DOI PMC

Round J. L., Mazmanian S. K. (2009). The gut microbiome shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313–323. 10.1038/nri2515 PubMed DOI PMC

Sak B., Petrzelkova K. J., Kvetonova D., Mynarova A., Shutt K. A., Pomajbikova K., et al. . (2013). Long-term monitoring of microsporidia, cryptosporidium and giardia infections in Western Lowland Gorillas (Gorilla gorilla gorilla) at different stages of habituation in Dzanga Sangha Protected Areas, Central African Republic. PLoS ONE 8:e71840. 10.1371/journal.pone.0071840 PubMed DOI PMC

Schloss P. D., Gevers D., Westcott S. L. (2011). Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS ONE 6:e27310. 10.1371/journal.pone.0027310 PubMed DOI PMC

Schnorr S. L., Candela M., Rampelli S., Centanni M., Consolandi C., Basaglia G., et al. . (2014). Gut microbiome of the Hadza hunter-gatherers. Nat. Commun. 5:3654. 10.1038/ncomms4654 PubMed DOI PMC

Seivwright L. J., Redpath S. M., Mougeot F., Watt L., Hudson P. J. (2004). Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J. Helminthol. 78, 69–76. 10.1079/JOH2003220 PubMed DOI

Sheather A. L. (1923). The detection of intestinal protozoa and mange parasites by a floatation technique. J. Pathol. Ther. 36, 266–275. 10.1016/S0368-1742(23)80052-2 DOI

Šlapeta J., Dowd S. E., Alanazi A. D., Westman M. E., Brown G. K. (2015). Differences in the faecal microbiome of non-diarrhoeic clinically healthy dogs and cats associated with Giardia duodenalis infection: impact of hookworms and coccidia. Int. J. Parasitol. 45, 585–594. 10.1016/j.ijpara.2015.04.001 PubMed DOI

Stensvold C. R., Lebbad M., Verweij J. J., Jespersgaard C., von Samson-Himmelstjerna G., Nielsen S. S., et al. . (2010). Identification and delineation of members of the Entamoeba complex by pyrosequencing. Mol. Cell. Probes 24, 403–406. 10.1016/j.mcp.2010.07.008 PubMed DOI

Su C., Cao Y., Kaplan J., Zhang M., Li W., Conroy M., et al. . (2011). Duodenal helminth infection alters barrier function of the colonic epithelium via adaptive immune activation. Infect. Immun. 79, 2285–2294. 10.1128/IAI.01123-10 PubMed DOI PMC

Summers R. W., Elliott D. E., U. J. F., Jr, Thompson R. A., Weinstock J. V. (2005). Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128, 825–832. 10.1053/j.gastro.2005.01.005 PubMed DOI

Tandon B. N., Tandon R. K., Satpathy B. K., Shriniwas (1977). Mechanism of malabsorption in giardiasis: a study of bacterial flora and bile salt deconjugation in upper jejunum. Gut 18, 176–181. 10.1136/gut.18.3.176 PubMed DOI PMC

Tomkins A. M., Wright S. G., Drasar B. S., James W. P. (1978). Bacterial colonization of jejunal mucosa in giardiasis. Trans. R. Soc. Trop. Med. Hyg. 72, 33–36. 10.1016/0035-9203(78)90294-8 PubMed DOI

Venables W. N., Ripley B. D. (2002). Modern Applied Statistics with S, 4th Edn. New York, NY: Springer.

Verma A. K., Verma R., Ahuja V., Paul J. (2012). Real-time analysis of gut flora in Entamoeba histolytica infected patients of Northern India. BMC Microbiol. 12:183 10.1186/1471-2180-12-183 PubMed DOI PMC

Verweij J. J., Laeijendecker D., Brienen E. A., van Lieshout L., Polderman A. M. (2003). Detection and identification of Entamoeba species in stool samples by a reverse line hybridization assay. J. Clin. Microbiol. 41, 5041–5045. 10.1128/JCM.41.11.5041-5045.2003 PubMed DOI PMC

Vlčková K., Gomez A., Petrželková K. J., Whittier C. A., Todd A. F., Yeoman C. J., et al. . (2016). Effect of antibiotic treatment on the gastrointestinal microbiome of free-ranging western lowland gorillas (Gorilla g. gorilla). Microb. Ecol. 72, 943–954. 10.1007/s00248-016-0745-5 PubMed DOI

Vlčková K., Kreisinger J., Pafčo B., Čížková D., Tagg N., Hehl A. B., et al. . (2018). Diversity of Entamoeba spp. in African great apes and humans: An insight from Illumina MiSeq high-throughput sequencing. Int. J. Parasitol. 48, 519–530. 10.1016/j.ijpara.2017.11.008 PubMed DOI

Walk S. T., Blum A. M., Ewing S. A.-S., Weinstock J. V., Young V. B. (2010). Alteration of the murine gut microbiota during infection with the parasitic helminth, Heligmosomoides polygyrus. Inflamm. Bowel Dis. 16, 1841–1849. 10.1002/ibd.21299 PubMed DOI PMC

Wang J., Tang H., Zhang C., Zhao Y., Derrien M., Rocher E., et al. . (2015). Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J. 9, 1–15. 10.1038/ismej.2014.99 PubMed DOI PMC

Wang Q., Garrity G. M., Tiedje J. M., Cole J. R. (2007). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267. 10.1128/AEM.00062-07 PubMed DOI PMC

Warnes G. R., Bolker B., Bonebakker L., Gentleman R., Liaw W. H. A., Lumley T., et al. (2016). Gplots: Various R Programming Tools for Plotting Data. R package version 3.0.1.

Warnick L. D. (1992). Daily variability of equine fecal strongyle egg counts. Cornell Vet. 82, 453–463. PubMed

Whelan R. A., Hartmann S., Rausch S. (2012). Nematode modulation of inflammatory bowel disease. Protoplasma 249, 871–886. 10.1007/s00709-011-0342-x PubMed DOI PMC

Wu S., Li R. W., Li W., Beshah E., Dawson H. D., Urban J. F., Jr. (2012). Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection. PLoS ONE 7:e35470. 10.1371/journal.pone.0035470 PubMed DOI PMC

Zaiss M. M., Harris N. L. (2016). Interactions between the intestinal microbiome and helminth parasites. Parasite Immunol. 38, 5–11. 10.1111/pim.12274 PubMed DOI PMC

Zajac A. M., Conboy G. A. (eds.). (2012). Veterinary Clinical Parasitology, 8th Edn. Chichester, UK: Wiley-Blackwell.

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