{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,20]],"date-time":"2026-01-20T01:23:59Z","timestamp":1768872239699,"version":"3.49.0"},"reference-count":60,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,4,6]],"date-time":"2021-04-06T00:00:00Z","timestamp":1617667200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,4,6]],"date-time":"2021-04-06T00:00:00Z","timestamp":1617667200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/L027186\/1"],"award-info":[{"award-number":["BB\/L027186\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004815","name":"Isaac Newton Trust","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100004815","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100010661","name":"Horizon 2020","doi-asserted-by":"crossref","award":["635408"],"award-info":[{"award-number":["635408"]}],"id":[{"id":"10.13039\/100010661","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Parasites Vectors"],"published-print":{"date-parts":[[2021,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec><jats:title>Background<\/jats:title><jats:p>Growing evidence points towards a role of gastrointestinal (GI) helminth parasites of ruminants in modifying the composition of the host gut flora, with likely repercussions on the pathophysiology of worm infection and disease, and on animal growth and productivity. However, a thorough understanding of the mechanisms governing helminth-microbiota interactions and of their impact on host health and welfare relies on reproducibility and replicability of findings. To this aim, in this study, we analysed quantitative and qualitative fluctuations in the faecal microbiota composition of lambs vaccinated against, and experimentally infected with, the parasitic GI nematode<jats:italic>Teladorsagia circumcincta<\/jats:italic>over the course of two separate trials performed over two\u00a0consecutive years.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Two trials were conducted under similar experimental conditions in 2017 and 2018, respectively. In each trial, lambs were randomly assigned to one of the following experimental groups: (i) vaccinated\/infected, (ii) unvaccinated\/infected and (iii) unvaccinated\/uninfected. Faecal samples collected from individual animals were subjected to DNA extraction followed by high-throughput sequencing of the V3-V4 region of the bacterial 16S rRNA gene and bioinformatics and biostatistical analyses of sequence data.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Substantial differences in the populations of bacteria affected by immunisation against and infection by<jats:italic>T. circumcincta<\/jats:italic>were detected when comparing data from the two trials. Nevertheless, the abundance of<jats:italic>Prevotella<\/jats:italic>spp. was significantly linked to helminth infection in both trials.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>Despite the largely conflicting findings between the two trials, our data revealed that selected gut microbial populations are consistently affected by<jats:italic>T. circumcincta<\/jats:italic>infection and\/or vaccination. Nevertheless, our study calls for caution when interpreting data generated from<jats:italic>in vivo<\/jats:italic>helminth-microbiome interaction studies that may be influenced by several intrinsic and extrinsic host-, parasite- and environment-related factors.<\/jats:p><\/jats:sec><jats:sec><jats:title>Graphical Abstract<\/jats:title><\/jats:sec>","DOI":"10.1186\/s13071-021-04688-4","type":"journal-article","created":{"date-parts":[[2021,4,6]],"date-time":"2021-04-06T19:03:01Z","timestamp":1617735781000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Vaccination against the brown stomach worm, Teladorsagia circumcincta, followed by parasite challenge, induces inconsistent modifications in gut microbiota composition of lambs"],"prefix":"10.1186","volume":"14","author":[{"given":"James","family":"Rooney","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alba","family":"Cort\u00e9s","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Riccardo","family":"Scotti","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniel R. G.","family":"Price","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yvonne","family":"Bartley","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Karen","family":"Fairlie-Clarke","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tom N.","family":"McNeilly","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alasdair J.","family":"Nisbet","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6863-2950","authenticated-orcid":false,"given":"Cinzia","family":"Cantacessi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2021,4,6]]},"reference":[{"key":"4688_CR1","doi-asserted-by":"crossref","first-page":"2853","DOI":"10.1098\/rstb.2010.0134","volume":"365","author":"PK Thornton","year":"2010","unstructured":"Thornton PK. Livestock production: recent trends, future prospects. Philos Trans R Soc B Biol Sci. 2010;365:2853\u201367.","journal-title":"Philos Trans R Soc B Biol Sci"},{"key":"4688_CR2","doi-asserted-by":"crossref","first-page":"20878","DOI":"10.1073\/pnas.1321844111","volume":"110","author":"M Herrero","year":"2013","unstructured":"Herrero M, Thornton PK. Livestock and global change: emerging issues for sustainable food systems. Proc Natl Acad Sci USA. 2013;110:20878\u201381.","journal-title":"Proc Natl Acad Sci USA"},{"key":"4688_CR3","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/j.pt.2014.04.009","volume":"30","author":"J Charlier","year":"2014","unstructured":"Charlier J, van der Voort M, Kenyon F, Skuce P, Vercruysse J. Chasing helminths and their economic impact on farmed ruminants. Trends Parasitol. 2014;30:361\u20137.","journal-title":"Trends Parasitol"},{"key":"4688_CR4","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.vetpar.2013.04.005","volume":"195","author":"JL Fitzpatrick","year":"2013","unstructured":"Fitzpatrick JL. Global food security: the impact of veterinary parasites and parasitologists. Vet Parasitol. 2013;195:233\u201348.","journal-title":"Vet Parasitol"},{"key":"4688_CR5","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.vetpar.2015.01.004","volume":"208","author":"V Molina-Hern\u00e1ndez","year":"2015","unstructured":"Molina-Hern\u00e1ndez V, Mulcahy G, P\u00e9rez J, Mart\u00ednez-Moreno \u00c1, Donnelly S, O\u2019Neill SM, Dalton JP, Cwiklinski K. Fasciola hepatica vaccine: we may not be there yet but we\u2019re on the right road. Vet Parasitol. 2015;208:101\u201311.","journal-title":"Vet Parasitol"},{"key":"4688_CR6","first-page":"135","volume":"3","author":"WFH Jarrett","year":"1960","unstructured":"Jarrett WFH, Jennings FW, McIntyre WIM, Mulligan W, Urquhart GM. Immunological studies on Dictyocaulus viviparus infection. Active immunization with whole worm vaccine. Immunology. 1960;3:135\u201344.","journal-title":"Immunology"},{"key":"4688_CR7","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/S0020-7519(00)00157-0","volume":"31","author":"JB Matthews","year":"2001","unstructured":"Matthews JB, Davidson AJ, Freeman KL, French NP. Immunisation of cattle with recombinant acetylcholinesterase from Dictyocaulus viviparus and with adult worm ES products. Int J Parasitol. 2001;31:307\u201317.","journal-title":"Int J Parasitol"},{"key":"4688_CR8","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1046\/j.1365-3024.2002.00461.x","volume":"24","author":"P Geldhof","year":"2002","unstructured":"Geldhof P, Claerebout E, Knox D, Vercauteren I, Looszova A, Vercruysse J. Vaccination of calves against Ostertagia ostertagi with cysteine proteinase enriched protein fractions. Parasite Immunol. 2002;24:263\u201370.","journal-title":"Parasite Immunol"},{"key":"4688_CR9","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/j.vetpar.2007.08.014","volume":"149","author":"Y Meyvis","year":"2007","unstructured":"Meyvis Y, Geldhof P, Gevaert K, Timmerman E, Vercruysse J, Claerebout E. Vaccination against Ostertagia ostertagi with subfractions of the protective ES-thiol fraction. Vet Parasitol. 2007;149:239\u201345.","journal-title":"Vet Parasitol"},{"key":"4688_CR10","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1016\/j.ijpara.2014.04.010","volume":"44","author":"CC Bassetto","year":"2014","unstructured":"Bassetto CC, Silva MRL, Newlands GFJ, Smith WD, Ratti JJ, Martins CL, Amarante AFT. Vaccination of grazing calves with antigens from the intestinal membranes of Haemonchus contortus: effects against natural challenge with Haemonchus placei and Haemonchus similis. Int J Parasitol. 2014;44:697\u2013702.","journal-title":"Int J Parasitol"},{"key":"4688_CR11","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1186\/s13071-015-0733-5","volume":"8","author":"C Strube","year":"2015","unstructured":"Strube C, Haake C, Sager H, Schorderet Weber S, Kaminsky R, Buschbaum S, Joekel D, Schicht S, Kremmer E, Korrell J, Schnieder T, von Samson-Himmelstjerna G. Vaccination with recombinant paramyosin against the bovine lungworm Dictyocaulus viviparus considerably reduces worm burden and larvae shedding. Parasit Vectors. 2015;8:119.","journal-title":"Parasit Vectors"},{"key":"4688_CR12","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/j.ijpara.2014.11.001","volume":"45","author":"J Vlaminck","year":"2015","unstructured":"Vlaminck J, Borloo J, Vercruysse J, Geldhof P, Claerebout E. Vaccination of calves against Cooperia oncophora with a double-domain activation-associated secreted protein reduces parasite egg output and pasture contamination. Int J Parasitol. 2015;45:209\u201313.","journal-title":"Int J Parasitol"},{"key":"4688_CR13","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.vetpar.2016.08.024","volume":"229","author":"L Meier","year":"2016","unstructured":"Meier L, Torgerson PR, Hertzberg H. Vaccination of goats against Haemonchus contortus with the gut membrane proteins H11\/H-gal-GP. Vet Parasitol. 2016;229:15\u201321.","journal-title":"Vet Parasitol"},{"key":"4688_CR14","doi-asserted-by":"crossref","first-page":"4017","DOI":"10.1016\/j.vaccine.2013.05.026","volume":"31","author":"AJ Nisbet","year":"2013","unstructured":"Nisbet AJ, McNeilly TN, Wildblood LA, Morrison AA, Bartley DJ, Bartley Y, Longhi C, McKendrick IJ, Palarea-Albaladejo J, Matthews JB. Successful immunization against a parasitic nematode by vaccination with recombinant proteins. Vaccine. 2013;31:4017\u201323.","journal-title":"Vaccine"},{"key":"4688_CR15","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.vetpar.2016.09.002","volume":"228","author":"AJ Nisbet","year":"2016","unstructured":"Nisbet AJ, McNeilly TN, Greer AW, Bartley Y, Oliver EM, Smith S, Palarea-Albaladejo J, Matthews JB. Protection of ewes against Teladorsagia circumcincta infection in the periparturient period by vaccination with recombinant antigens. Vet Parasitol. 2016;228:130\u20136.","journal-title":"Vet Parasitol"},{"key":"4688_CR16","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.ijpara.2018.10.006","volume":"49","author":"AJ Nisbet","year":"2019","unstructured":"Nisbet AJ, McNeilly TN, Price DRG, Oliver EM, Bartley Y, Mitchell M, Palarea-Albaladejo J, Matthews JB. The rational simplification of a recombinant cocktail vaccine to control the parasitic nematode Teladorsagia circumcincta. Int J Parasitol. 2019;49:257\u201365.","journal-title":"Int J Parasitol"},{"key":"4688_CR17","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1079\/ASC41010023","volume":"81","author":"GJ Nieuwhof","year":"2005","unstructured":"Nieuwhof GJ, Bishop SC. Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact. Anim Sci. 2005;81:23\u20139.","journal-title":"Anim Sci"},{"key":"4688_CR18","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1016\/j.ijpara.2014.07.011","volume":"44","author":"H Toet","year":"2014","unstructured":"Toet H, Piedrafita DM, Spithill TW. Liver fluke vaccines in ruminants: strategies, progress and future opportunities. Int J Parasitol. 2014;44:915\u201327.","journal-title":"Int J Parasitol"},{"key":"4688_CR19","doi-asserted-by":"crossref","first-page":"e1003000","DOI":"10.1371\/journal.ppat.1003000","volume":"8","author":"MJ Broadhurst","year":"2012","unstructured":"Broadhurst MJ, Ardeshir A, Kanwar B, Mirpuri J, Gundra UM, Leung JM, Wiens KE, Vujkovic-Cvijin I, Kim CC, Yarovinsky F, Lerche NW, McCune JM, Loke P. Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog. 2012;8:e1003000.","journal-title":"PLoS Pathog"},{"key":"4688_CR20","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1038\/s41385-018-0008-5","volume":"11","author":"TP Brosschot","year":"2018","unstructured":"Brosschot TP, Reynolds LA. The impact of a helminth-modified microbiome on host immunity. Mucosal Immunol. 2018;11:1039\u201346.","journal-title":"Mucosal Immunol"},{"key":"4688_CR21","doi-asserted-by":"crossref","first-page":"1028","DOI":"10.3389\/fgene.2019.01028","volume":"10","author":"I Martin","year":"2019","unstructured":"Martin I, Kaisar MMM, Wiria AE, Hamid F, Djuardi Y, Sartono E, Rosa BA, Mitreva M, Supali T, Houwing-Duistermaat JJ, Yazdanbakhsh M, Wammes LJ. The effect of gut microbiome composition on human immune responses: an exploration of interference by helminth infections. Front Genet. 2019;10:1028.","journal-title":"Front Genet"},{"key":"4688_CR22","doi-asserted-by":"crossref","first-page":"e24417","DOI":"10.1371\/journal.pone.0024417","volume":"6","author":"RW Li","year":"2011","unstructured":"Li RW, Wu S, Li W, Huang Y, Gasbarre LC. Metagenome plasticity of the bovine abomasal microbiota in immune animals in response to Ostertagia ostertagi infection. PLoS ONE. 2011;6:e24417.","journal-title":"PLoS ONE"},{"key":"4688_CR23","doi-asserted-by":"crossref","first-page":"20606","DOI":"10.1038\/srep20606","volume":"6","author":"RW Li","year":"2016","unstructured":"Li RW, Li W, Sun J, Yu P, Baldwin RL, Urban JF. The effect of helminth infection on the microbial composition and structure of the caprine abomasal microbiome. Sci Rep. 2016;6:20606.","journal-title":"Sci Rep"},{"key":"4688_CR24","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/s11259-017-9698-5","volume":"41","author":"S El-Ashram","year":"2017","unstructured":"El-Ashram S, Al Nasr I, Abouhajer F, El-Kemary M, Huang G, Din\u00e7el G, Mehmood R, Hu M, Suo X. Microbial community and ovine host response varies with early and late stages of Haemonchus contortus infection. Vet Res Commun. 2017;41:263\u201377.","journal-title":"Vet Res Commun"},{"key":"4688_CR25","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1186\/s40168-020-00818-9","volume":"8","author":"A Cort\u00e9s","year":"2020","unstructured":"Cort\u00e9s A, Wills J, Su X, Hewitt RE, Robertson J, Scotti R, Price DRG, Bartley Y, McNeilly TN, Krause L, Powell JJ, Nisbet AJ, Cantacessi C. Infection with the sheep gastrointestinal nematode Teladorsagia circumcincta increases luminal pathobionts. Microbiome. 2020;8:60.","journal-title":"Microbiome"},{"key":"4688_CR26","doi-asserted-by":"crossref","first-page":"e2880","DOI":"10.1371\/journal.pntd.0002880","volume":"8","author":"SC Lee","year":"2014","unstructured":"Lee SC, Tang MS, Lim YAL, Choy SH, Kurtz ZD, Cox LM, Gundra UM, Cho I, Bonneau R, Blaser MJ, Chua KH, Loke P. Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl Trop Dis. 2014;8:e2880.","journal-title":"PLoS Negl Trop Dis"},{"key":"4688_CR27","doi-asserted-by":"crossref","first-page":"e0159770","DOI":"10.1371\/journal.pone.0159770","volume":"11","author":"IM Cattadori","year":"2016","unstructured":"Cattadori IM, Sebastian A, Hao H, Katani R, Albert I, Eilertson KE, Kapur V, Pathak A, Mitchell S. Impact of helminth infections and nutritional constraints on the small intestine microbiota. PLoS ONE. 2016;11:e0159770.","journal-title":"PLoS ONE"},{"key":"4688_CR28","doi-asserted-by":"crossref","first-page":"1371","DOI":"10.1017\/S003118201900088X","volume":"146","author":"A Cort\u00e9s","year":"2019","unstructured":"Cort\u00e9s A, Peachey LE, Jenkins TP, Scotti R, Cantacessi C. Helminths and microbes within the vertebrate gut\u2014not all studies are created equal. Parasitology. 2019;146:1371\u20138.","journal-title":"Parasitology"},{"key":"4688_CR29","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1038\/nmeth.f.303","volume":"7","author":"JG Caporaso","year":"2010","unstructured":"Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pe\u00f1a AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335\u20136.","journal-title":"Nat Methods"},{"key":"4688_CR30","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1038\/nmeth.3869","volume":"13","author":"BJ Callahan","year":"2016","unstructured":"Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581\u20133.","journal-title":"Nat Methods"},{"key":"4688_CR31","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1093\/bioinformatics\/btw725","volume":"33","author":"M Zakrzewski","year":"2017","unstructured":"Zakrzewski M, Proietti C, Ellis JJ, Hasan S, Brion M-J, Berger B, Krause L. Calypso: a user-friendly web-server for mining and visualizing microbiome-environment interactions. Bioinformatics. 2017;33:782\u20133.","journal-title":"Bioinformatics"},{"key":"4688_CR32","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1111\/j.1442-9993.1993.tb00438.x","volume":"18","author":"KR Clarke","year":"1993","unstructured":"Clarke KR. Non-parametric multivariate analyses of changes in community structure. Aust J Ecol. 1993;18:117\u201343.","journal-title":"Aust J Ecol"},{"key":"4688_CR33","first-page":"32","volume":"26","author":"MJ Anderson","year":"2001","unstructured":"Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;26:32\u201346.","journal-title":"Austral Ecol"},{"key":"4688_CR34","doi-asserted-by":"crossref","first-page":"R60","DOI":"10.1186\/gb-2011-12-6-r60","volume":"12","author":"N Segata","year":"2011","unstructured":"Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.","journal-title":"Genome Biol"},{"key":"4688_CR35","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/s40168-019-0782-7","volume":"8","author":"R Scotti","year":"2020","unstructured":"Scotti R, Southern S, Boinett C, Jenkins TP, Cort\u00e9s A, Cantacessi C. MICHELINdb: a web-based tool for mining of helminth-microbiota interaction datasets, and a meta-analysis of current research. Microbiome. 2020;8:10.","journal-title":"Microbiome"},{"key":"4688_CR36","doi-asserted-by":"crossref","first-page":"e0160169","DOI":"10.1371\/journal.pone.0160169","volume":"11","author":"KA L\u00ea Cao","year":"2016","unstructured":"L\u00ea Cao KA, Costello ME, Lakis VA, Bartolo F, Chua XY, Brazeilles R, Rondeau P. MixMC: a multivariate statistical framework to gain insight into microbial communities. PLoS ONE. 2016;11:e0160169.","journal-title":"PLoS ONE"},{"key":"4688_CR37","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.anaerobe.2006.12.001","volume":"13","author":"K Tajima","year":"2007","unstructured":"Tajima K, Nonaka I, Higuchi K, Takusari N, Kurihara M, Takenaka A, Mitsumori M, Kajikawa H, Aminov RI. Influence of high temperature and humidity on rumen bacterial diversity in Holstein heifers. Anaerobe. 2007;13:57\u201364.","journal-title":"Anaerobe"},{"key":"4688_CR38","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1159\/000365054","volume":"24","author":"NR Parmar","year":"2014","unstructured":"Parmar NR, Solanki JV, Patel AB, Shah TM, Patel AK, Parnerkar S, Kumar JIN, Joshi CG. Metagenome of Mehsani buffalo rumen microbiota: an assessment of variation in feed-dependent phylogenetic and functional classification. J Mol Microbiol Biotechnol. 2014;24:249\u201361.","journal-title":"J Mol Microbiol Biotechnol"},{"key":"4688_CR39","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1186\/s40168-017-0378-z","volume":"5","author":"MD Auffret","year":"2017","unstructured":"Auffret MD, Dewhurst RJ, Duthie CA, Rooke JA, Wallace JR, Freeman TC, Stewart R, Watson M, Roehe R. The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle. Microbiome. 2017;5:159.","journal-title":"Microbiome"},{"key":"4688_CR40","doi-asserted-by":"crossref","first-page":"3717","DOI":"10.1007\/s00253-017-8144-5","volume":"101","author":"Y Wang","year":"2017","unstructured":"Wang Y, Cao P, Wang L, Zhao Z, Chen Y, Yang Y. Bacterial community diversity associated with different levels of dietary nutrition in the rumen of sheep. Appl Microbiol Biotechnol. 2017;101:3717\u201328.","journal-title":"Appl Microbiol Biotechnol"},{"key":"4688_CR41","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1186\/s40168-017-0274-6","volume":"5","author":"SM Wolff","year":"2017","unstructured":"Wolff SM, Ellison MJ, Hao Y, Cockrum RR, Austin KJ, Baraboo M, Burch K, Lee HJ, Maurer T, Patil R, Ravelo A, Taxis TM, Truong H, Lamberson WR, Cammack KM, Conant GC. Diet shifts provoke complex and variable changes in the metabolic networks of the ruminal microbiome. Microbiome. 2017;5:60.","journal-title":"Microbiome"},{"key":"4688_CR42","doi-asserted-by":"crossref","first-page":"16612","DOI":"10.1038\/s41598-019-53279-y","volume":"9","author":"K Cui","year":"2019","unstructured":"Cui K, Qi M, Wang S, Diao Q, Zhang N. Dietary energy and protein levels influenced the growth performance, ruminal morphology and fermentation and microbial diversity of lambs. Sci Rep. 2019;9:16612.","journal-title":"Sci Rep"},{"key":"4688_CR43","doi-asserted-by":"crossref","first-page":"36","DOI":"10.3389\/fvets.2015.00036","volume":"2","author":"N Malmuthuge","year":"2015","unstructured":"Malmuthuge N, Griebel PJ, Guan LL. The gut microbiome and its potential role in the development and function of newborn calf gastrointestinal tract. Front Vet Sci. 2015;2:36.","journal-title":"Front Vet Sci"},{"key":"4688_CR44","doi-asserted-by":"crossref","first-page":"19620","DOI":"10.1038\/s41598-019-56206-3","volume":"9","author":"L Wang","year":"2019","unstructured":"Wang L, Zhang K, Zhang C, Feng Y, Zhang X, Wang X, Wu G. Dynamics and stabilization of the rumen microbiome in yearling Tibetan sheep. Sci Rep. 2019;9:19620.","journal-title":"Sci Rep"},{"key":"4688_CR45","doi-asserted-by":"crossref","first-page":"75","DOI":"10.3390\/microorganisms6030075","volume":"6","author":"SY Geerlings","year":"2018","unstructured":"Geerlings SY, Kostopoulos I, de Vos WM, Belzer C. Akkermansia muciniphila in the human gastrointestinal tract: when, where, and how? Microorganisms. 2018;6:75.","journal-title":"Microorganisms"},{"key":"4688_CR46","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1186\/s12917-019-2031-5","volume":"15","author":"G Chang","year":"2019","unstructured":"Chang G, Zhang H, Wang Y, Ma N, Chandra RA, Ye G, Zhuang S, Zhu W, Shen X. Microbial community shifts elicit inflammation in the caecal mucosa via the GPR41\/43 signalling pathway during subacute ruminal acidosis. BMC Vet Res. 2019;15:298.","journal-title":"BMC Vet Res"},{"key":"4688_CR47","doi-asserted-by":"crossref","first-page":"e0186752","DOI":"10.1371\/journal.pone.0186752","volume":"12","author":"I Scott","year":"2017","unstructured":"Scott I, Umair S, Savoian MS, Simpson HV. Abomasal dysfunction and cellular and mucin changes during infection of sheep with larval or adult Teladorsagia circumcincta. PLoS ONE. 2017;12:e0186752.","journal-title":"PLoS ONE"},{"key":"4688_CR48","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.vetpar.2008.12.023","volume":"161","author":"A Rowe","year":"2009","unstructured":"Rowe A, Gondro C, Emery D, Sangster N. Sequential microarray to identify timing of molecular responses to Haemonchus contortus infection in sheep. Vet Parasitol. 2009;161:76\u201387.","journal-title":"Vet Parasitol"},{"key":"4688_CR49","doi-asserted-by":"publisher","DOI":"10.1101\/845511","author":"J Gerritsen","year":"2019","unstructured":"Gerritsen J, Hornung B, Ritari J, Paulin L, Rijkers GT, Schaap PJ, de Vos WM, Smidt H. A comparative and functional genomics analysis of the genus Romboutsia provides insight into adaptation to an intestinal lifestyle. bioRxiv. 2019. https:\/\/doi.org\/10.1101\/845511.","journal-title":"bioRxiv"},{"key":"4688_CR50","doi-asserted-by":"crossref","first-page":"2509","DOI":"10.3389\/fmicb.2018.02509","volume":"9","author":"Y Wang","year":"2018","unstructured":"Wang Y, Zhang H, Zhu L, Xu Y, Liu N, Sun X, Hu L, Huang H, Wei K, Zhu R. Dynamic distribution of gut microbiota in goats at different ages and health states. Front Microbiol. 2018;9:2509.","journal-title":"Front Microbiol"},{"key":"4688_CR51","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.femsec.2004.05.005","volume":"50","author":"I Mangin","year":"2004","unstructured":"Mangin I, Bonnet R, Seksik P, Rigottier-Gois L, Sutren M, Bouhnik Y, Neut C, Collins MD, Colombel JF, Marteau P. Dor\u00e9. Molecular inventory of faecal microflora in patients with Crohn\u2019s disease. FEMS Microbiol Ecol. 2004;50:25\u201336.","journal-title":"FEMS Microbiol Ecol."},{"key":"4688_CR52","doi-asserted-by":"crossref","first-page":"1844","DOI":"10.1111\/jgh.14281","volume":"33","author":"YJ Chen","year":"2018","unstructured":"Chen YJ, Wu H, Wu SD, Lu N, Wang YT, Liu HN, Dong L, Liu TT, Shen XZ. Parasutterella, in association with irritable bowel syndrome and intestinal chronic inflammation. J Gastroenterol Hepatol. 2018;33:1844\u201352.","journal-title":"J Gastroenterol Hepatol"},{"key":"4688_CR53","doi-asserted-by":"crossref","first-page":"e1005939","DOI":"10.1371\/journal.pcbi.1005939","volume":"14","author":"R Menon","year":"2018","unstructured":"Menon R, Ramanan V, Korolev KS. Interactions between species introduce spurious associations in microbiome studies. PLoS Comput Biol. 2018;14:e1005939.","journal-title":"PLoS Comput Biol"},{"key":"4688_CR54","doi-asserted-by":"crossref","first-page":"e27076","DOI":"10.1371\/journal.pone.0027076","volume":"6","author":"I Mukhopadhya","year":"2011","unstructured":"Mukhopadhya I, Hansen R, Nicholl CE, Alhaidan YA, Thomson JM, Berry SH, Pattinson C, Stead DA, Russell RK, El-Omar EM, Hold GL. A comprehensive evaluation of colonic mucosal isolates of Sutterella wadsworthensis from inflammatory bowel disease. PLoS ONE. 2011;6:e27076.","journal-title":"PLoS ONE"},{"key":"4688_CR55","doi-asserted-by":"crossref","first-page":"1706","DOI":"10.3389\/fmicb.2016.01706","volume":"7","author":"K Hiippala","year":"2016","unstructured":"Hiippala K, Kainulainen V, Kalliom\u00e4ki M, Arkkila P, Satokari R. Mucosal prevalence and interactions with the epithelium indicate commensalism of Sutterella spp. Front Microbiol. 2016;7:1706.","journal-title":"Front Microbiol"},{"key":"4688_CR56","doi-asserted-by":"crossref","first-page":"4097","DOI":"10.5433\/1679-0359.2016v37n6p4097","volume":"37","author":"A Tirabassi","year":"2016","unstructured":"Tirabassi A, Madeira H, Fragoso S, Umaki A, Egevardt R, Melo T, Pereira J, Teixeira V, Ollhoff D, Sotomaior C. Molecular identification of abomasal bacteria associated with resistance and susceptibility to Haemonchus contortus infection in sheep. Semina Ci\u00eanc Agr\u00e1r. 2016;37:4097\u2013108.","journal-title":"Semina Ci\u00eanc Agr\u00e1r"},{"key":"4688_CR57","doi-asserted-by":"crossref","first-page":"998","DOI":"10.1016\/j.immuni.2015.09.012","volume":"43","author":"MM Zaiss","year":"2015","unstructured":"Zaiss MM, Rapin A, Lebon L, Dubey LK, Mosconi I, Sarter K, Piersigilli A, Menin L, Walker AW, Rougemont J, Paerewijck O, Geldhof P, McCoy KD, Macpherson AJ, Croese J, Giacomin PR, Loukas A, Junt T, Marsland BJ, Harris NL. The intestinal microbiota contributes to the ability of helminths to modulate allergic inflammation. Immunity. 2015;43:998\u20131010.","journal-title":"Immunity"},{"key":"4688_CR58","doi-asserted-by":"crossref","first-page":"277","DOI":"10.3389\/fimmu.2019.00277","volume":"10","author":"PD Venegas","year":"2019","unstructured":"Venegas PD, De la Fuente MK, Landskron G, Gonz\u00e1lez MJ, Quera R, Dijkstra G, Harmsen HJM, Faber KN, Hermoso MA. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol. 2019;10:277.","journal-title":"Front Immunol"},{"key":"4688_CR59","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1080\/14787210.2020.1782188","volume":"5","author":"A Cort\u00e9s","year":"2020","unstructured":"Cort\u00e9s A, Rooney J, Bartley DJ, Nisbet AJ, Cantacessi C. Helminths, hosts, and their microbiota: new avenues for managing gastrointestinal helminthiases in ruminants. Expert Rev Anti Infect Ther. 2020;5:977\u201385.","journal-title":"Expert Rev Anti Infect Ther."},{"key":"4688_CR60","doi-asserted-by":"crossref","first-page":"80","DOI":"10.4172\/1948-5948.1000126","volume":"6","author":"S Huws","year":"2014","unstructured":"Huws S, Mayorga O, Theodorou M, Kim EJ, Cookson A, Newbold C, Kingston-Smith AH. Differential colonization of plant parts by the rumen microbiota is likely to be due to different forage chemistries. J Microb Biochem Technol. 2014;6:80\u20136.","journal-title":"J Microb Biochem Technol"}],"container-title":["Parasites &amp; Vectors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13071-021-04688-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13071-021-04688-4\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13071-021-04688-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,1]],"date-time":"2023-11-01T18:56:47Z","timestamp":1698865007000},"score":1,"resource":{"primary":{"URL":"https:\/\/parasitesandvectors.biomedcentral.com\/articles\/10.1186\/s13071-021-04688-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,6]]},"references-count":60,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,12]]}},"alternative-id":["4688"],"URL":"https:\/\/doi.org\/10.1186\/s13071-021-04688-4","relation":{},"ISSN":["1756-3305"],"issn-type":[{"value":"1756-3305","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,6]]},"assertion":[{"value":"12 February 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 March 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 April 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All experimental procedures described here were approved by the Moredun Research Institute Experiments and Ethics Committee, UK, and were conducted under the legislation of UK Home Office Project Licenses (references PPL 60\/4238 and 70\/8870) in accordance with the Animals (Scientific Procedures) Act of 1986.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"189"}}