{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,5]],"date-time":"2026-06-05T20:38:57Z","timestamp":1780691937588,"version":"3.54.1"},"reference-count":116,"publisher":"MDPI AG","issue":"21","license":[{"start":{"date-parts":[[2022,11,1]],"date-time":"2022-11-01T00:00:00Z","timestamp":1667260800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"University of Cartagena","award":["BPIN20200000100405"],"award-info":[{"award-number":["BPIN20200000100405"]}]},{"name":"Colombian Ministry of Science (Minciencias)","award":["BPIN20200000100405"],"award-info":[{"award-number":["BPIN20200000100405"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Humans have coexisted with helminths and bacteria for the entire existence of our species. Nowadays, helminth infections affect more than 1.9 billion people worldwide, especially in underdeveloped regions that lack optimal sanitary conditions. In addition, commensal microorganisms inhabit several compartments of humans, including the gastrointestinal tract, constituting what we know as the microbiota. Helminths and bacterial microbiota can interact in various ways. In this review, the interactions between helminths and commensal bacteria are analyzed in both animal models and humans. In developing countries, the gut microbiota exhibits high diversity, which could be linked to the high burden of helminthiasis in these areas. In fact, several studies show that helminth infections are associated with an increased gut microbiota diversity and changes in its composition. Interestingly, these changes can modify the risk for some diseases, such as asthma, colitis, viral infections, and metabolic conditions. Besides, the microbiota is necessary for the establishment of some helminth infections and can also influence the evolution of these diseases. Specific bacterial taxa can contribute to the resistance or susceptibility to certain helminths. The mechanisms underlying helminth\u2013microbiota interactions are not completely understood. More research is necessary to address this and other unmet needs, especially considering that available studies are heterogeneous and sometimes yield conflicting results.<\/jats:p>","DOI":"10.3390\/ijms232113358","type":"journal-article","created":{"date-parts":[[2022,11,2]],"date-time":"2022-11-02T03:36:44Z","timestamp":1667360204000},"page":"13358","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":34,"title":["Helminths and Bacterial Microbiota: The Interactions of Two of Humans\u2019 \u201cOld Friends\u201d"],"prefix":"10.3390","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5331-7410","authenticated-orcid":false,"given":"Kevin","family":"Llin\u00e1s-Caballero","sequence":"first","affiliation":[{"name":"Institute for Immunological Research, University of Cartagena, Cartagena 130014, Colombia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5204-1109","authenticated-orcid":false,"given":"Luis","family":"Caraballo","sequence":"additional","affiliation":[{"name":"Institute for Immunological Research, University of Cartagena, Cartagena 130014, Colombia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,11,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1186\/s13059-015-0759-1","article-title":"Host genetic variation impacts microbiome composition across human body sites","volume":"16","author":"Blekhman","year":"2015","journal-title":"Genome Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1413","DOI":"10.1038\/ng.3693","article-title":"Association of host genome with intestinal microbial composition in a large healthy cohort","volume":"48","author":"Turpin","year":"2016","journal-title":"Nat. Genet."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1396","DOI":"10.1038\/ng.3695","article-title":"Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota","volume":"48","author":"Wang","year":"2016","journal-title":"Nat. Genet."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1079","DOI":"10.1038\/s41564-020-0743-8","article-title":"Genome-wide associations of human gut microbiome variation and implications for causal inference analyses","volume":"5","author":"Hughes","year":"2020","journal-title":"Nat. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1038\/s41588-020-00763-1","article-title":"Large-scale association analyses identify host factors influencing human gut microbiome composition","volume":"53","author":"Kurilshikov","year":"2021","journal-title":"Nat. Genet."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1111\/j.1365-2249.2010.04133.x","article-title":"99th Dahlem Conference on Infection, Inflammation and Chronic Inflammatory Disorders: Darwinian medicine and the \u2018hygiene\u2019 or \u2018old friends\u2019 hypothesis","volume":"160","author":"Rook","year":"2010","journal-title":"Clin. Exp. Immunol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1126\/science.ada1336","article-title":"Microbiome data dominated by wealthy countries","volume":"375","author":"Ortega","year":"2022","journal-title":"Science"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1038\/s41586-022-04427-4","article-title":"The lung microbiome regulates brain autoimmunity","volume":"603","author":"Hosang","year":"2022","journal-title":"Nature"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.actatropica.2018.07.016","article-title":"Ascaris lumbricoides infection induces both, reduction and increase of asthma symptoms in a rural community","volume":"187","author":"Zakzuk","year":"2018","journal-title":"Acta Trop."},{"key":"ref_10","first-page":"1960","article-title":"Ascaris exposure and its association with lung function, asthma, and DNA methylation in Northern Europe","volume":"149","author":"Kitaba","year":"2021","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"9582","DOI":"10.1038\/s41598-018-27964-3","article-title":"Gut microbiota components are associated with fixed airway obstruction in asthmatic patients living in the tropics","volume":"8","author":"Zakzuk","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_12","unstructured":"The World Bank (2022, July 03). World Bank Country and Lending Groups. Available online: https:\/\/datahelpdesk.worldbank.org\/knowledgebase\/articles\/906519-world-bank-country-and-lending-groups."},{"key":"ref_13","unstructured":"The World Bank (2022, July 03). Population, Total-Low & Middle Income. Available online: https:\/\/data.worldbank.org\/indicator\/SP.POP.TOTL?locations=XO."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"The Human Microbiome Project Consortium (2012). Structure, function and diversity of the healthy human microbiome. Nature, 486, 207\u2013214.","DOI":"10.1038\/nature11234"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1038\/s41586-020-2881-9","article-title":"Host variables confound gut microbiota studies of human disease","volume":"587","author":"Sklar","year":"2020","journal-title":"Nature"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1038\/nature11053","article-title":"Human gut microbiome viewed across age and geography","volume":"486","author":"Yatsunenko","year":"2012","journal-title":"Nature"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1016\/j.celrep.2015.03.049","article-title":"The Gut Microbiota of Rural Papua New Guineans: Composition, Diversity Patterns, and Ecological Processes","volume":"11","author":"Stegen","year":"2015","journal-title":"Cell Rep."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Lee, S.C., Tang, M.S., Lim, Y.A.L., Choy, S.H., Kurtz, Z.D., Cox, L.M., Gundra, U.M., Cho, I., Bonneau, R., and Blaser, M.J. (2014). Helminth Colonization Is Associated with Increased Diversity of the Gut Microbiota. PLoS Negl. Trop. Dis., 8.","DOI":"10.1371\/journal.pntd.0002880"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s40168-018-0416-5","article-title":"Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia","volume":"6","author":"Rosa","year":"2018","journal-title":"Microbiome"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1126\/science.aan4834","article-title":"Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania","volume":"357","author":"Smits","year":"2017","journal-title":"Science"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"14691","DOI":"10.1073\/pnas.1005963107","article-title":"Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa","volume":"107","author":"Cavalieri","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Jha, A.R., Davenport, E.R., Gautam, Y., Bhandari, D., Tandukar, S., Ng, K.M., Fragiadakis, G.K., Holmes, S., Gautam, G.P., and Leach, J. (2018). Gut microbiome transition across a lifestyle gradient in Himalaya. PLoS Biol., 16.","DOI":"10.1101\/253450"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1038\/nature17672","article-title":"Interconnected microbiomes and resistomes in low-income human habitats","volume":"533","author":"Pehrsson","year":"2016","journal-title":"Nature"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"962","DOI":"10.1016\/j.cell.2018.10.029","article-title":"US Immigration Westernizes the Human Gut Microbiome","volume":"175","author":"Vangay","year":"2018","journal-title":"Cell"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/19490976.2021.1902705","article-title":"The Impact of Migration on the Gut Metagenome of South Asian Canadians","volume":"13","author":"Copeland","year":"2021","journal-title":"Gut Microbes"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Amaruddin, A.I., Hamid, F., Koopman, J.P.R., Muhammad, M., Brienen, E.A.T., van Lieshout, L., Geelen, A.R., Wahyuni, S., Kuijper, E.J., and Sartono, E. (2020). The Bacterial Gut Microbiota of Schoolchildren from High and Low Socioeconomic Status: A Study in an Urban Area of Makassar, Indonesia. Microorganisms, 8.","DOI":"10.3390\/microorganisms8060961"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"242","DOI":"10.3201\/eid2101.140795","article-title":"Microbiota That Affect Risk for Shigellosis in Children in Low-Income Countries","volume":"21","author":"Lindsay","year":"2015","journal-title":"Emerg. Infect. Dis."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/gb-2014-15-6-r76","article-title":"Diarrhea in young children from low-income countries leads to large-scale alterations in wintestinal microbiota composition","volume":"15","author":"Pop","year":"2014","journal-title":"Genome Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2282","DOI":"10.3389\/fimmu.2018.02282","article-title":"Parasitic Nematodes Exert Antimicrobial Activity and Benefit from Microbiota-Driven Support for Host Immune Regulation","volume":"9","author":"Rausch","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"522","DOI":"10.4161\/gmic.32155","article-title":"Commensal-pathogen interactions in the intestinal tract","volume":"5","author":"Reynolds","year":"2014","journal-title":"Gut Microbes"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1391","DOI":"10.1126\/science.1187703","article-title":"Exploitation of the Intestinal Microflora by the Parasitic Nematode Trichuris muris","volume":"328","author":"Hayes","year":"2010","journal-title":"Science"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1126\/sciadv.aap7399","article-title":"Manipulation of host and parasite microbiotas: Survival strategies during chronic nematode infection","volume":"4","author":"White","year":"2018","journal-title":"Sci. Adv."},{"key":"ref_33","doi-asserted-by":"crossref","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","year":"2008","journal-title":"Int. Immunopharmacol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"118719","DOI":"10.1016\/j.carbpol.2021.118719","article-title":"\u03b2-Glucan-triggered Akkermansia muciniphila expansion facilitates the expulsion of intestinal helminth via TLR2 in mice","volume":"275","author":"Jin","year":"2022","journal-title":"Carbohydr. Polym."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.ppat.1008066","article-title":"Linking the effects of helminth infection, diet and the gut microbiota with human whole-blood signatures","volume":"15","author":"Lee","year":"2019","journal-title":"PLoS Pathog."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1042\/BJ20050218","article-title":"Cecropin P1 and novel nematode cecropins: A bacteria-inducible antimicrobial peptide family in the nematode Ascaris suum","volume":"390","author":"Pillai","year":"2005","journal-title":"Biochem. J."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1006\/expr.2001.4643","article-title":"Trichuris suis: Detection of antibacterial activity in excretory-secretory products from adults","volume":"99","author":"Abner","year":"2001","journal-title":"Exp. Parasitol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1038\/s41396-020-0589-3","article-title":"The gut microbiota response to helminth infection depends on host sex and genotype","volume":"14","author":"Ling","year":"2020","journal-title":"ISME J."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"20140295","DOI":"10.1098\/rstb.2014.0295","article-title":"Interactions between multiple helminths and the gut microbiota in wild rodents","volume":"370","author":"Kreisinger","year":"2015","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1841","DOI":"10.1002\/ibd.21299","article-title":"Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus","volume":"16","author":"Walk","year":"2010","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1186\/s40168-015-0103-8","article-title":"Type 2 immunity-dependent reduction of segmented filamentous bacteria in mice infected with the helminthic parasite Nippostrongylus brasiliensis","volume":"3","author":"Fricke","year":"2015","journal-title":"Microbiome"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.ijpara.2019.09.005","article-title":"Infection with a small intestinal helminth, Heligmosomoides polygyrus bakeri, consistently alters microbial communities throughout the murine small and large intestine","volume":"50","author":"Rapin","year":"2020","journal-title":"Int. J. Parasitol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0074026","article-title":"Small Intestinal Nematode Infection of Mice Is Associated with Increased Enterobacterial Loads alongside the Intestinal Tract","volume":"8","author":"Rausch","year":"2013","journal-title":"PLoS ONE"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.ijpara.2018.10.007","article-title":"Ascaris suum infection was associated with a worm-independent reduction in microbial diversity and altered metabolic potential in the porcine gut microbiome","volume":"49","author":"Wang","year":"2019","journal-title":"Int. J. Parasitol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1","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":"ref_46","doi-asserted-by":"crossref","first-page":"637570","DOI":"10.3389\/fcimb.2021.637570","article-title":"Whipworm-Associated Intestinal Microbiome Members Consistent Across Both Human and Mouse Hosts","volume":"11","author":"Rosa","year":"2021","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Houlden, A., Hayes, K.S., Bancroft, A.J., Worthington, J.J., Wang, P., Grencis, R.K., and Roberts, I.S. (2015). Chronic Trichuris muris infection in C57BL\/6 mice causes significant changes in host microbiota and metabolome: Effects reversed by pathogen clearance. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0125945"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0125495","article-title":"Chronic Trichuris muris infection decreases diversity of the intestinal microbiota and concomitantly increases the abundance of lactobacilli","volume":"10","author":"Holm","year":"2015","journal-title":"PLoS ONE"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"2150","DOI":"10.1128\/IAI.00141-12","article-title":"Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis","volume":"80","author":"Li","year":"2012","journal-title":"Infect. Immun."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Wu, S., Li, R.W., Li, W., Beshah, E., Dawson, H.D., and Urban, J.F. (2012). Worm Burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0035470"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"312","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":"ref_52","doi-asserted-by":"crossref","first-page":"e00642-19","DOI":"10.1128\/IAI.00642-19","article-title":"Whipworm Infection Promotes Bacterial Invasion, Intestinal Microbiota Imbalance, and Cellular Immunomodulation","volume":"88","author":"Schachter","year":"2020","journal-title":"Infect. Immun."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/pim.12721","article-title":"Preconception helminth infection alters offspring microbiota and immune subsets in a mouse model","volume":"42","author":"Nyangahu","year":"2020","journal-title":"Parasite Immunol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"e02890-21","DOI":"10.1128\/mBio.02890-21","article-title":"Helminth-Induced Human Gastrointestinal Dysbiosis: A Systematic Review and Meta-Analysis Reveals Insights into Altered Taxon Diversity and Microbial Gradient Collapse","volume":"12","author":"Kupritz","year":"2021","journal-title":"mBio"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/j.ijpara.2019.12.008","article-title":"Helminths, polyparasitism, and the gut microbiome in the Philippines","volume":"50","author":"Gordon","year":"2020","journal-title":"Int. J. Parasitol."},{"key":"ref_56","first-page":"1","article-title":"Intestinal parasitic infection alters bacterial gut microbiota in children","volume":"2019","author":"Alzate","year":"2019","journal-title":"PeerJ"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1126\/science.aaf3229","article-title":"Helminth infection promotes colonization resistance via type 2 immunity","volume":"352","author":"Ramanan","year":"2016","journal-title":"Science"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1486","DOI":"10.4269\/ajtmh.18-0968","article-title":"Interactions between parasitic infections and the human gut microbiome in Odisha, India","volume":"100","author":"Huwe","year":"2019","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0184719","article-title":"Infections by human gastrointestinal helminths are associated with changes in faecal microbiota diversity and composition","volume":"12","author":"Jenkins","year":"2017","journal-title":"PLoS ONE"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Cooper, P., Walker, A.W., Reyes, J., Chico, M., Salter, S.J., Vaca, M., and Parkhill, J. (2013). Patent Human Infections with the Whipworm, Trichuris trichiura, Are Not Associated with Alterations in the Faecal Microbiota. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0076573"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Pane, S., Sacco, A., Iorio, A., Romani, L., and Putignani, L. (2021). Strongyloides stercoralis infestation in a child: How a nematode can affect gut microbiota. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22042131"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1051\/parasite\/2020074","article-title":"Alteration of the fecal microbiota in Chinese patients with Schistosoma japonicum infection","volume":"28","author":"Jiang","year":"2021","journal-title":"Parasite"},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Kay, G.L., Millard, A., Sergeant, M.J., Midzi, N., Gwisai, R., Mduluza, T., Ivens, A., Nausch, N., Mutapi, F., and Pallen, M. (2015). Differences in the faecal microbiome in schistosoma haematobium infected children vs. uninfected children. PLoS Negl. Trop. Dis., 9.","DOI":"10.1371\/journal.pntd.0003861"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"2292","DOI":"10.3389\/fmicb.2018.02292","article-title":"Altered Gut Microbiota Composition in Subjects Infected with Clonorchis sinensis","volume":"9","author":"Xu","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"972","DOI":"10.1017\/S0031182020000736","article-title":"Intestinal parasites in rural communities in Nan Province, Thailand: Changes in bacterial gut microbiota associated with minute intestinal fluke infection","volume":"147","author":"Prommi","year":"2020","journal-title":"Parasitology"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/mBio.00519-19","article-title":"The impact of anthelmintic treatment on human gut microbiota based on cross-sectional and pre-and postdeworming comparisons in Western Kenya","volume":"10","author":"Easton","year":"2019","journal-title":"mBio"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"3504","DOI":"10.1128\/IAI.67.7.3504-3511.1999","article-title":"Differential roles of segmented filamentous bacteria and clostridia in development of the intestinal immune system","volume":"67","author":"Umesaki","year":"1999","journal-title":"Infect. Immun."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"16731","DOI":"10.1073\/pnas.0804812105","article-title":"Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients","volume":"105","author":"Sokol","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1126\/science.1198469","article-title":"Induction of colonic regulatory T cells by indigenous Clostridium species","volume":"331","author":"Atarashi","year":"2011","journal-title":"Science"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1097\/01.MIB.0000440815.76627.64","article-title":"The commensal bacterium Faecalibacterium prausnitzii is protective in DNBS-induced chronic moderate and severe colitis models","volume":"20","author":"Martin","year":"2014","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/j.immuni.2014.06.015","article-title":"Bacterial Sensor Nod2 Prevents Inflammation of the Small Intestine by Restricting the Expansion of the Commensal Bacteroides vulgatus","volume":"41","author":"Ramanan","year":"2014","journal-title":"Immunity"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1186\/s40168-021-01146-2","article-title":"Cooperation between host immunity and the gut bacteria is essential for helminth-evoked suppression of colitis","volume":"9","author":"Shute","year":"2021","journal-title":"Microbiome"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1038\/mi.2017.20","article-title":"Helminth-induced alterations of the gut microbiota exacerbate bacterial colitis","volume":"11","author":"Su","year":"2018","journal-title":"Mucosal Immunol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"998","DOI":"10.1016\/j.immuni.2015.09.012","article-title":"The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation","volume":"43","author":"Zaiss","year":"2015","journal-title":"Immunity"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"763","DOI":"10.1016\/j.jcmgh.2020.06.010","article-title":"Helminth-Induced and Th2-Dependent Alterations of the Gut Microbiota Attenuate Obesity Caused by High-Fat Diet","volume":"10","author":"Su","year":"2020","journal-title":"Cell. Mol. Gastroenterol. Hepatol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.ijpara.2020.07.012","article-title":"Trichinella spiralis infection ameliorated diet-induced obesity model in mice","volume":"51","author":"Kang","year":"2021","journal-title":"Int. J. Parasitol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"606530","DOI":"10.3389\/fendo.2020.606530","article-title":"Gastrointestinal Helminth Infection Improves Insulin Sensitivity, Decreases Systemic Inflammation, and Alters the Composition of Gut Microbiota in Distinct Mouse Models of Type 2 Diabetes","volume":"11","author":"Khudhair","year":"2021","journal-title":"Front. Endocrinol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.phrs.2018.04.008","article-title":"Helminth infection in mice improves insulin sensitivity via modulation of gut microbiota and fatty acid metabolism","volume":"132","author":"Pace","year":"2018","journal-title":"Pharmacol. Res."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1068","DOI":"10.1016\/j.jaci.2017.01.016","article-title":"Enteric helminth-induced type I interferon signaling protects against pulmonary virus infection through interaction with the microbiota","volume":"140","author":"McFarlane","year":"2017","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1016\/j.jaci.2014.07.022","article-title":"Experimental hookworm infection and gluten microchallenge promote tolerance in celiac disease","volume":"135","author":"Croese","year":"2015","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1431","DOI":"10.1093\/infdis\/jiu256","article-title":"Impact of experimental hookworm infection on the human gut microbiota","volume":"210","author":"Cantacessi","year":"2014","journal-title":"J. Infect. Dis."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"13797","DOI":"10.1038\/srep13797","article-title":"Experimental hookworm infection and escalating gluten challenges are associated with increased microbial richness in celiac subjects","volume":"5","author":"Giacomin","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/srep36797","article-title":"Changes in duodenal tissue-associated microbiota following hookworm infection and consecutive gluten challenges in humans with coeliac disease","volume":"6","author":"Giacomin","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1016\/j.jaci.2011.04.060","article-title":"Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age","volume":"128","author":"Bisgaard","year":"2011","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1111\/j.1365-2222.2008.03156.x","article-title":"Altered early infant gut microbiota in children developing allergy up to 5 years of age","volume":"39","author":"Jenmalm","year":"2009","journal-title":"Clin. Exp. Allergy"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1016\/j.jaci.2011.10.025","article-title":"Low diversity of the gut microbiota in infants with atopic eczema","volume":"129","author":"Abrahamsson","year":"2012","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1038\/nature12506","article-title":"Richness of human gut microbiome correlates with metabolic markers","volume":"500","author":"Nielsen","year":"2013","journal-title":"Nature"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1053\/j.gastro.2011.04.011","article-title":"Twin Study Indicates Loss of Interaction Between Microbiota and Mucosa of Patients with Ulcerative Colitis","volume":"141","author":"Lepage","year":"2011","journal-title":"Gastroenterology"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1136\/gut.2005.073817","article-title":"Reduced diversity of faecal microbiota in Crohn\u2019s disease revealed by a metagenomic approach","volume":"55","author":"Manichanh","year":"2006","journal-title":"Gut"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1016\/S0140-6736(14)60460-8","article-title":"Global, regional, and national prevalence of overweight and obesity in children and adults during 1980\u20132013: A systematic analysis for the Global Burden of Disease Study 2013","volume":"384","author":"Ng","year":"2014","journal-title":"Lancet"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/S2468-1253(19)30333-4","article-title":"The global, regional, and national burden of inflammatory bowel disease in 195 countries and territories, 1990\u20132017: A systematic analysis for the Global Burden of Disease Study 2017","volume":"5","author":"Alatab","year":"2020","journal-title":"Lancet Gastroenterol. Hepatol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1093\/ije\/30.1.173","article-title":"The relationship of per capita gross national product to the prevalence of symptoms of asthma and other atopic diseases in children (ISAAC)","volume":"30","author":"Stewart","year":"2001","journal-title":"Int. J. Epidemiol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.aller.2012.03.001","article-title":"The International Study of Asthma and Allergies in Childhood (ISAAC) Phase Three: A global synthesis","volume":"41","author":"Mallol","year":"2013","journal-title":"Allergol. Immunopathol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"150","DOI":"10.4168\/aair.2012.4.3.150","article-title":"Asthma Prevention by Lactobacillus Rhamnosus in a Mouse Model is Associated with CD4 + CD25 + Foxp3 + T Cells","volume":"4","author":"Jang","year":"2012","journal-title":"Allergy Asthma Immunol. Res."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1164\/rccm.200806-951OC","article-title":"Lactobacillus reuteri \u2013induced Regulatory T cells Protect against an Allergic Airway Response in Mice","volume":"179","author":"Karimi","year":"2009","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"672","DOI":"10.1111\/j.1600-0625.2012.01539.x","article-title":"A novel mouse model of atopic dermatitis with epicutaneous allergen sensitization and the effect of Lactobacillus rhamnosus","volume":"21","author":"Kim","year":"2012","journal-title":"Exp. Dermatol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1205","DOI":"10.1016\/j.freeradbiomed.2009.07.033","article-title":"Lactobacillus rhamnosus blocks inflammatory signaling in vivo via reactive oxygen species generation","volume":"47","author":"Lin","year":"2009","journal-title":"Free Radic. Biol. Med."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"e170","DOI":"10.1111\/j.1365-2567.2008.02942.x","article-title":"A component of polysaccharide peptidoglycan complex on Lactobacillus induced an improvement of murine model of inflammatory bowel disease and colitis-associated cancer","volume":"128","author":"Matsumoto","year":"2009","journal-title":"Immunology"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1038\/nature12726","article-title":"Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation","volume":"504","author":"Arpaia","year":"2013","journal-title":"Nature"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1038\/nature12721","article-title":"Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells","volume":"504","author":"Furusawa","year":"2013","journal-title":"Nature"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1126\/science.1241165","article-title":"The Microbial Metabolites, Short-Chain Fatty Acids, Regulate Colonic T reg Cell Homeostasis","volume":"341","author":"Smith","year":"2013","journal-title":"Science"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1038\/nature10434","article-title":"Peripheral education of the immune system by colonic commensal microbiota","volume":"478","author":"Lathrop","year":"2011","journal-title":"Nature"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"989","DOI":"10.1126\/science.aac4263","article-title":"The microbiota regulates type 2 immunity through ROR t+ T cells","volume":"349","author":"Ohnmacht","year":"2015","journal-title":"Science"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"277","DOI":"10.3389\/fimmu.2019.00277","article-title":"Short Chain Fatty Acids (SCFAs)-Mediated Gut Epithelial and Immune Regulation and Its Relevance for Inflammatory Bowel Diseases","volume":"10","author":"Landskron","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"1469","DOI":"10.1099\/ijs.0.02873-0","article-title":"Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium","volume":"54","author":"Derrien","year":"2004","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"33","DOI":"10.3164\/jcbn.18-57","article-title":"A next-generation beneficial microbe: Akkermansia muciniphila","volume":"63","author":"Naito","year":"2018","journal-title":"J. Clin. Biochem. Nutr."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1016\/j.ijpara.2009.12.006","article-title":"Acetate formation in the energy metabolism of parasitic helminths and protists","volume":"40","author":"Tielens","year":"2010","journal-title":"Int. J. Parasitol."},{"key":"ref_108","doi-asserted-by":"crossref","unstructured":"Acevedo, N., Alhamwe, B.A., Caraballo, L., Ding, M., Ferrante, A., Garn, H., Garssen, J., Hii, C.S., Irvine, J., and Llin\u00e1s-Caballero, K. (2021). Perinatal and early-life nutrition, epigenetics, and allergy. Nutrients, 13.","DOI":"10.3390\/nu13030724"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"7320","DOI":"10.1038\/ncomms8320","article-title":"Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites","volume":"6","author":"Thorburn","year":"2015","journal-title":"Nat. Commun."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"756","DOI":"10.3389\/fimmu.2020.00756","article-title":"IgE Levels to Ascaris and House Dust Mite Allergens Are Associated with Increased Histone Acetylation at Key Type-2 Immune Genes","volume":"11","author":"Zakzuk","year":"2020","journal-title":"Front. Immunol."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"271","DOI":"10.3389\/fcimb.2018.00271","article-title":"The Intestinal Roundworm Ascaris suum Releases Antimicrobial Factors Which Interfere with Bacterial Growth and Biofilm Formation","volume":"8","author":"Midha","year":"2018","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_112","doi-asserted-by":"crossref","unstructured":"Midha, A., Goyette-Desjardins, G., Goerdeler, F., Moscovitz, O., Seeberger, P.H., Tedin, K., Bertzbach, L.D., Lepenies, B., and Hartmann, S. (2021). Lectin-Mediated Bacterial Modulation by the Intestinal Nematode Ascaris suum. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22168739"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"1578116","DOI":"10.1080\/20013078.2019.1578116","article-title":"Exploration of extracellular vesicles from Ascaris suum provides evidence of parasite-host cross talk","volume":"8","author":"Hansen","year":"2019","journal-title":"J. Extracell. Vesicles"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1016\/j.pt.2022.06.003","article-title":"Parasitic helminths and the host microbiome-a missing \u2019extracellular vesicle-sized\u2019 link?","volume":"38","author":"Rooney","year":"2022","journal-title":"Trends Parasitol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"eabe6723","DOI":"10.1126\/science.abe6723","article-title":"Small proline-rich protein 2A is a gut bactericidal protein deployed during helminth infection","volume":"374","author":"Hu","year":"2021","journal-title":"Science"},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"941530","DOI":"10.3389\/fimmu.2022.941530","article-title":"Potential Gut Microbiota Features for Non-Invasive Detection of Schistosomiasis","volume":"13","author":"Lin","year":"2022","journal-title":"Front. Immunol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/21\/13358\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:08:55Z","timestamp":1760144935000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/21\/13358"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,1]]},"references-count":116,"journal-issue":{"issue":"21","published-online":{"date-parts":[[2022,11]]}},"alternative-id":["ijms232113358"],"URL":"https:\/\/doi.org\/10.3390\/ijms232113358","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,11,1]]}}}