{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T19:33:17Z","timestamp":1789155197573,"version":"build-2803163510"},"reference-count":46,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,1,5]],"date-time":"2022-01-05T00:00:00Z","timestamp":1641340800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100008393","name":"Teknologi og Produktion, Det Frie Forskningsr\u00e5d","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100008393","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"abstract":"<jats:p>\n                    Dietary probiotics may enhance gut health by directly competing with pathogenic agents and through immunostimulatory effects. These properties are recognized in the context of bacterial and viral pathogens, but less is known about interactions with eukaryotic pathogens such as parasitic worms (helminths). In this study we investigated whether two probiotic mixtures (comprised of\n                    <jats:italic>Bacillus amyloliquefaciens, B. subtilis<\/jats:italic>\n                    , and\n                    <jats:italic>Enterococcus faecium<\/jats:italic>\n                    [BBE], or\n                    <jats:italic>Lactobacillus rhamnosus<\/jats:italic>\n                    LGG and\n                    <jats:italic>Bifidobacterium animalis<\/jats:italic>\n                    subspecies\n                    <jats:italic>Lactis<\/jats:italic>\n                    Bb12 [LB]) could modulate helminth infection kinetics as well as the gut microbiome and intestinal immune responses in pigs infected with the nodular worm\n                    <jats:italic>Oesophagostomum dentatum<\/jats:italic>\n                    . We observed that neither probiotic mixture influenced helminth infection levels. BBE, and to a lesser extent LB, changed the alpha- and beta-diversity indices of the colon and fecal microbiota, notably including an enrichment of fecal\n                    <jats:italic>Bifidobacterium<\/jats:italic>\n                    spp. by BBE. However, these effects were muted by concurrent\n                    <jats:italic>O. dentatum<\/jats:italic>\n                    infection. BBE (but not LB) significantly attenuated the\n                    <jats:italic>O. dentatum<\/jats:italic>\n                    -induced upregulation of genes involved in type-2 inflammation and restored normal lymphocyte ratios in the ileo-caecal lymph nodes that were altered by infection. Moreover, inflammatory cytokine release from blood mononuclear cells and intestinal lymphocytes was diminished by BBE. Collectively, our data suggest that selected probiotic mixtures can play a role in maintaining immune homeostasis during type 2-biased inflammation. In addition, potentially beneficial changes in the microbiome induced by dietary probiotics may be counteracted by helminths, highlighting the complex inter-relationships that potentially exist between probiotic bacteria and intestinal parasites.\n                  <\/jats:p>","DOI":"10.3389\/fimmu.2021.793260","type":"journal-article","created":{"date-parts":[[2022,1,5]],"date-time":"2022-01-05T00:51:01Z","timestamp":1641343861000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":25,"title":["Parasite-Probiotic Interactions in the Gut: Bacillus sp. and Enterococcus faecium Regulate Type-2 Inflammatory Responses and Modify the Gut Microbiota of Pigs During Helminth Infection"],"prefix":"10.3389","volume":"12","author":[{"given":"Laura J.","family":"Myhill","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sophie","family":"Stolzenbach","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helena","family":"Mejer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lukasz","family":"Krych","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simon R.","family":"Jakobsen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Witold","family":"Kot","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kerstin","family":"Skovgaard","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nuria","family":"Canibe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Nejsum","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dennis S.","family":"Nielsen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stig M.","family":"Thamsborg","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew R.","family":"Williams","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,1,5]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"111222","DOI":"10.1016\/j.molbiopara.2019.111222","article-title":"Helminth-Microbiota Cross-Talk \u2013 A Journey Through the Vertebrate Digestive System","volume":"233","author":"Cort\u00e9s","year":"2019","journal-title":"Mol\u00a0Biochem Parasitol"},{"key":"B2","article-title":"Probiotics in Food - Health and Nutritional Properties and Guidelines for Evaluation","volume-title":"FAO Food and Nutrition Paper 85","year":"2006"},{"key":"B3","doi-asserted-by":"publisher","first-page":"610769","DOI":"10.1155\/2011\/610769","article-title":"Probiotics for the Control of Parasites: An Overview","volume":"2011","author":"Travers","year":"2011","journal-title":"J Parasitol Res"},{"key":"B4","doi-asserted-by":"publisher","first-page":"16161","DOI":"10.1038\/nmicrobiol.2016.161","article-title":"A Reference Gene Catalogue of the Pig Gut Microbiome","volume":"1","author":"Xiao","year":"2016","journal-title":"Nat Microbiol"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1111\/j.1439-0396.2005.00601.x","article-title":"Dietary Probiotic Supplementation and Resulting Effects on Performance, Health Status, and Microbial Characteristics of Primiparous Sows","volume":"90","author":"B\u00f6hmer","year":"2006","journal-title":"J Anim Physiol Anim Nutr (Berl.)"},{"key":"B6","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1186\/1746-6148-8-89","article-title":"Effects of Lactobacillus Plantarum ZJ316 on Pig Growth and Pork Quality","volume":"8","author":"Suo","year":"2012","journal-title":"BMC Vet Res"},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.3389\/fvets.2019.00026","article-title":"Effects of Dietary Supplementation With Enterococcus Faecium and Clostridium Butyricum, Either Alone or in Combination, on Growth and Fecal Microbiota Composition of Post-Weaning Pigs at a Commercial Farm","volume":"6","author":"Sato","year":"2019","journal-title":"Front Vet Sci"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1093\/jas\/skz235","article-title":"Effects of Clostridium Butyricum and Enterococcus Faecalis on Growth Performance, Intestinal Structure, and Inflammation in Lipopolysaccharide-Challenged Weaned Piglets","volume":"97","author":"Wang","year":"2019","journal-title":"J Anim Sci"},{"key":"B9","doi-asserted-by":"publisher","first-page":"599","DOI":"10.1111\/j.1574-6941.2008.00517.x","article-title":"Feeding of Lactobacillus Sobrius Reduces Escherichia Coli F4 Levels in the Gut and Promotes Growth of Infected Piglets","volume":"66","author":"Konstantinov","year":"2008","journal-title":"FEMS Microbiol Ecol"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.67.11.5037-5042.2001","article-title":"Inhibition of Giardia Intestinalis by Extracellular Factors From Lactobacilli: An In Vitro Study","volume":"67","author":"P\u00e9rez","year":"2001","journal-title":"Appl Environ Microbiol"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1007\/s00436-016-5196-x","article-title":"Prebiotic Inulin Supplementation Modulates the Immune Response and Restores Gut Morphology in Giardia Duodenalis-Infected Malnourished Mice","volume":"115","author":"Shukla","year":"2016","journal-title":"Parasitol Res"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1093\/jn\/135.5.1171","article-title":"Enterococcus Faecium SF68 Enhances the Immune Response to Giardia Intestinalis in Mice","volume":"135","author":"Benyacoub","year":"2005","journal-title":"J Nutr"},{"key":"B13","doi-asserted-by":"publisher","first-page":"e0007201","DOI":"10.1371\/journal.pntd.0007201","article-title":"Challenges and Opportunities for Control and Elimination of Soil-Transmitted Helminth Infection Beyond 2020","volume":"13","author":"Freeman","year":"2019","journal-title":"PLoS Negl Trop Dis"},{"key":"B14","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1016\/j.pt.2018.10.006","article-title":"100 Questions in Livestock Helminthology Research","volume":"35","author":"Morgan","year":"2019","journal-title":"Trends Parasitol"},{"key":"B15","doi-asserted-by":"publisher","first-page":"e1283385","DOI":"10.1080\/21688370.2017.1283385","article-title":"Helminths and Intestinal Barrier Function","volume":"5","author":"McKay","year":"2017","journal-title":"Tissue Barriers"},{"key":"B16","article-title":"Dose Related Mucosal Hyperplasia Induced by Oesophagostomum Dentatum Infection in Pigs","volume":"61","author":"Jensen","year":"1997","journal-title":"Can J Vet Res"},{"key":"B17","doi-asserted-by":"publisher","first-page":"e16577","DOI":"10.1371\/journal.pone.0016577","article-title":"Lactobacillus Rhamnosus HN001 Attenuates Allergy Development in a Pig Model","volume":"6","author":"Thomas","year":"2011","journal-title":"PLoS One"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1017\/S0031182003003251","article-title":"The Effect of Inulin and Sugar Beet Fibre on Oesophagostomum Dentatum Infection in Pigs","volume":"127","author":"Petkevicius","year":"2003","journal-title":"Parasitology"},{"key":"B19","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1016\/j.vetpar.2004.03.008","article-title":"Effects of Short-Chain Fatty Acids and Lactic Acids on Survival of Oesophagostomum Dentatum in Pigs","volume":"122","author":"Petkevicius","year":"2004","journal-title":"Vet Parasitol"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2018.02557","article-title":"Mucosal Barrier and Th2 Immune Responses Are Enhanced by Dietary Inulin in Pigs Infected With Trichuris Suis","volume":"9","author":"Myhill","year":"2018","journal-title":"Front Immunol"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2020.00312","article-title":"Dietary Inulin and Trichuris Suis Infection Promote Beneficial Bacteria Throughout the Porcine Gut","volume":"11","author":"Stolzenbach","year":"2020","journal-title":"Front Microbiol"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1080\/19490976.2018.1460014","article-title":"Bifidobacterium Animalis Subspecies Lactis Modulates the Local Immune Response and Glucose Uptake in the Small Intestine of Juvenile Pigs Infected With the Parasitic Nematode Ascaris Suum","volume":"9","author":"Solano-Aguilar","year":"2018","journal-title":"Gut Microbes"},{"key":"B23","doi-asserted-by":"publisher","first-page":"1113","DOI":"10.3390\/nu9101113","article-title":"Flavanol-Rich Cocoa Powder Interacts With Lactobacillus Rhamnossus LGG to Alter the Antibody Response to Infection With the Parasitic Nematode Ascaris Suum","volume":"9","author":"Jang","year":"2017","journal-title":"Nutrients"},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1016\/j.vetpar.2014.12.005","article-title":"Immune and Inflammatory Responses in Pigs Infected With Trichuris Suis and Oesophagostomum Dentatum","volume":"207","author":"Andreasen","year":"2015","journal-title":"Vet Parasitol"},{"key":"B25","first-page":"35","article-title":"Chapter 3: Faecal Examinations for Parasites","volume-title":"FAO Animal Health Manual 3: Epidemiology, Diagnosis and Control of Helminth Parasites in Swine.","author":"Roepstorff","year":"1998"},{"key":"B26","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1016\/j.livsci.2007.01.095","article-title":"Fermented Liquid Feed and Fermented Grain to Piglets- Effect on Gastrointestinal Ecology and Growth Performance","volume":"108","author":"Canibe","year":"2007","journal-title":"Livestock Sci"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1016\/0304-4017(95)00916-7","article-title":"Recovery of Oesophagostomum Dentatum From Pigs by Isolation of Parasites Migrating From Large Intestinal Contents Embedded in Agar-Gel","volume":"63","author":"Slotved","year":"1996","journal-title":"Vet Parasitol"},{"key":"B28","doi-asserted-by":"publisher","first-page":"e0186546","DOI":"10.1371\/journal.pone.0186546","article-title":"A Polyphenol-Enriched Diet and Ascaris Suum Infection Modulate Mucosal Immune Responses and Gut Microbiota Composition in Pigs","volume":"12","author":"Williams","year":"2017","journal-title":"PLoS One"},{"key":"B29","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1051\/vetres\/2009006","article-title":"Rapid and Widely Disseminated Acute Phase Protein Response After Experimental Bacterial Infection of Pigs","volume":"40","author":"Skovgaard","year":"2009","journal-title":"Vet Res"},{"key":"B30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.mimet.2017.10.015","article-title":"Have You Tried Spermine? A Rapid and Cost-Effective Method to Eliminate Dextran Sodium Sulfate Inhibition of PCR and RT-PCR","volume":"144","author":"Krych","year":"2018","journal-title":"J Microbiol Methods"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.f.303","article-title":"QIIME Allows Analysis of High-Throughput Community Sequencing Data","volume":"7","author":"Caporaso","year":"2010","journal-title":"Nat Methods"},{"key":"B32","doi-asserted-by":"publisher","first-page":"e0146312","DOI":"10.1371\/journal.pone.0146312","article-title":"Dietary Lactobacillus Rhamnosus GG Supplementation Improves the Mucosal Barrier Function in the Intestine of Weaned Piglets Challenged by Porcine Rotavirus","volume":"11","author":"Mao","year":"2016","journal-title":"PLoS One"},{"key":"B33","doi-asserted-by":"publisher","first-page":"e0199640","DOI":"10.1371\/journal.pone.0199640","article-title":"Alterations in the Gut Bacterial Microbiome in Fungal Keratitis Patients","volume":"13","author":"Kalyana Chakravarthy","year":"2018","journal-title":"PLoS One"},{"key":"B34","doi-asserted-by":"publisher","first-page":"4178986","DOI":"10.1155\/2018\/4178986","article-title":"Probiotics for the Control of Helminth Zoonosis","volume":"2018","author":"Reda","year":"2018","journal-title":"J Vet Med"},{"key":"B35","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1016\/j.intimp.2007.10.003","article-title":"Enhanced Susceptibility to Trichuris Muris Infection of B10Br Mice Treated With the Probiotic Lactobacillus Casei","volume":"8","author":"Dea-Ayuela","year":"2008","journal-title":"Int Immunopharmacol"},{"key":"B36","doi-asserted-by":"publisher","first-page":"818","DOI":"10.1128\/CVI.00047-13","article-title":"Lactobacillus Rhamnosus Ingestion Promotes Innate Host Defense in an Enteric Parasitic Infection","volume":"20","author":"McClemens","year":"2013","journal-title":"Clin Vaccine Immunol"},{"key":"B37","doi-asserted-by":"publisher","first-page":"41395","DOI":"10.1038\/srep41395","article-title":"Microbial Shifts in the Porcine Distal Gut in Response to Diets Supplemented With Enterococcus Faecalis as Alternatives to Antibiotics","volume":"7","author":"Li","year":"2017","journal-title":"Sci Rep"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1016\/j.cvfa.2019.08.004","article-title":"Nutraceuticals: An Alternative Strategy for the Use of Antimicrobials","volume":"35","author":"Ballou","year":"2019","journal-title":"Vet Clin North Am: Food Anim Pract"},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.1093\/advances\/nmy063","article-title":"Mechanisms of Action of Probiotics","volume":"10","author":"Plaza-Diaz","year":"2019","journal-title":"Adv Nutr"},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.1016\/j.vetpar.2004.05.011","article-title":"Symposium: New Approaches in the Study of Animal Parasites","volume":"125","author":"Klei","year":"2004","journal-title":"Vet Parasitol"},{"key":"B41","doi-asserted-by":"publisher","first-page":"e13439","DOI":"10.1111\/asj.13439","article-title":"Lactobacillus Rhamnosus GG Promotes M1 Polarization in Murine Bone Marrow-Derived Macrophages by Activating TLR2\/MyD88\/MAPK Signaling Pathway","volume":"91","author":"Wang","year":"2020","journal-title":"Anim Sci J"},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.1111\/lam.13255","article-title":"Lactobacillus Rhamnosus GG Components, SLP, gDNA and CpG, Exert Protective Effects on Mouse Macrophages Upon Lipopolysaccharide Challenge","volume":"70","author":"Qi","year":"2020","journal-title":"Lett Appl Microbiol"},{"key":"B43","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1186\/s13567-015-0223-y","article-title":"Oral Administration of a Select Mixture of Bacillus Probiotics Generates Tr1 Cells in Weaned F4ab\/acR\u2013 Pigs Challenged With an F4+ ETEC\/VTEC\/EPEC Strain","volume":"46","author":"Zhou","year":"2015","journal-title":"Vet Res"},{"key":"B44","doi-asserted-by":"publisher","first-page":"65","DOI":"10.4014\/jmb.1708.08051","article-title":"Preventive Effects of a Probiotic Mixture in an Ovalbumin-Induced Food Allergy Model","volume":"28","author":"Shin","year":"2018","journal-title":"J Microbiol Biotechnol"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1016\/j.jff.2016.06.006","article-title":"The Probiotic Activity of Lactobacillus Murinus Against Food Allergy","volume":"25","author":"Huang","year":"2016","journal-title":"J Funct Foods"},{"key":"B46","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1111\/j.1398-9995.2010.02501.x","article-title":"Oral Therapeutic Administration of a Probiotic Mixture Suppresses Established Th2 Responses and Systemic Anaphylaxis in a Murine Model of Food Allergy","volume":"66","author":"Schiavi","year":"2011","journal-title":"Allergy"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2021.793260\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,1,5]],"date-time":"2022-01-05T00:51:04Z","timestamp":1641343864000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2021.793260\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,5]]},"references-count":46,"alternative-id":["10.3389\/fimmu.2021.793260"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2021.793260","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.09.01.458597","asserted-by":"object"}]},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,5]]},"article-number":"793260"}}