{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T13:10:28Z","timestamp":1790946628472,"version":"4.1.0"},"reference-count":78,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2020,2,6]],"date-time":"2020-02-06T00:00:00Z","timestamp":1580947200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>The impact of the gut microbiome is being increasingly appreciated in health and in various chronic diseases, among them neurodegenerative disorders such as Parkinson\u2019s disease (PD). In the pathogenesis of PD, the role of the gut has been previously established. In conjunction with a better understanding of the intestinal microbiome, a link to the misfolding and spread of alpha-synuclein via inflammatory processes within the gut is discussed. In a case-control study, we assessed the gut microbiome of 54 PD patients and 32 healthy controls (HC). Additionally, we tested in this proof-of-concept study whether dietary intervention alone or additional physical colon cleaning may lead to changes of the gut microbiome in PD. 16 PD patients underwent a well-controlled balanced, ovo-lacto vegetarian diet intervention including short fatty acids for 14 days. 10 of those patients received additional treatment with daily fecal enema over 8 days. Stool samples were collected before and after 14 days of intervention. In comparison to HC, we could confirm previously reported PD associated microbiome changes. The UDPRS III significantly improved and the levodopa-equivalent daily dose decreased after vegetarian diet and fecal enema in a one-year follow-up. Additionally, we observed a significant association between the gut microbiome diversity and the UPDRS III and the abundance of Ruminococcaceae. Additionally, the abundance of Clostridiaceae was significantly reduced after enema. Dietary intervention and bowel cleansing may provide an additional non-pharmacologic therapeutic option for PD patients.<\/jats:p>","DOI":"10.3390\/cells9020376","type":"journal-article","created":{"date-parts":[[2020,2,7]],"date-time":"2020-02-07T03:13:27Z","timestamp":1581045207000},"page":"376","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":111,"title":["Interventional Influence of the Intestinal Microbiome Through Dietary Intervention and Bowel Cleansing Might Improve Motor Symptoms in Parkinson\u2019s Disease"],"prefix":"10.3390","volume":"9","author":[{"given":"Tobias","family":"Hegelmaier","sequence":"first","affiliation":[{"name":"Department of Neurology, Ruhr-University Bochum, St. Josef-Hospital Bochum, Bochum, 44791, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marco","family":"Lebbing","sequence":"additional","affiliation":[{"name":"Clinic of Neurology II, EVK Hattingen, Hattingen 45525, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander","family":"Duscha","sequence":"additional","affiliation":[{"name":"Department of Neurology, Ruhr-University Bochum, St. Josef-Hospital Bochum, Bochum, 44791, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura","family":"Tomaske","sequence":"additional","affiliation":[{"name":"Department of Neurology, Ruhr-University Bochum, St. Josef-Hospital Bochum, Bochum, 44791, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6621-144X","authenticated-orcid":false,"given":"Lars","family":"T\u00f6nges","sequence":"additional","affiliation":[{"name":"Department of Neurology, Ruhr-University Bochum, St. Josef-Hospital Bochum, Bochum, 44791, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacob Bak","family":"Holm","sequence":"additional","affiliation":[{"name":"Clinical Microbiomics A\/S, Copenhagen 2200, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Henrik","family":"Bj\u00f8rn Nielsen","sequence":"additional","affiliation":[{"name":"Clinical Microbiomics A\/S, Copenhagen 2200, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S\u00f6ren G.","family":"Gatermann","sequence":"additional","affiliation":[{"name":"Department of Medical Microbiology, Ruhr-University Bochum, Bochum, 44801, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Horst","family":"Przuntek","sequence":"additional","affiliation":[{"name":"Clinic of Neurology II, EVK Hattingen, Hattingen 45525, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aiden","family":"Haghikia","sequence":"additional","affiliation":[{"name":"Department of Neurology, Ruhr-University Bochum, St. Josef-Hospital Bochum, Bochum, 44791, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,2,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1111\/j.1468-1331.2008.02056.x","article-title":"Non-motor symptoms in Parkinson\u2019s disease","volume":"15","author":"Poewe","year":"2008","journal-title":"Eur. J. Neurol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1002\/mds.25150","article-title":"Parkinson\u2019s disease: Evidence for environmental risk factors","volume":"28","author":"Kieburtz","year":"2013","journal-title":"Mov. Disord. Off. J. Mov. Disord. Soc."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1332","DOI":"10.1007\/s00415-012-6801-2","article-title":"Gastrointestinal manifestations in Parkinson\u2019s disease: Prevalence and occurrence before motor symptoms","volume":"260","author":"Cersosimo","year":"2013","journal-title":"J. Neurol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1002\/mds.26942","article-title":"Parkinson\u2019s disease and Parkinson\u2019s disease medications have distinct signatures of the gut microbiome","volume":"32","author":"Debelius","year":"2017","journal-title":"Mov. Disord."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"734","DOI":"10.1007\/s10517-017-3700-7","article-title":"Analysis of Gut Microbiota in Patients with Parkinson\u2019s Disease","volume":"162","author":"Petrov","year":"2017","journal-title":"Bull. Exp. Biol. Med."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Hasegawa, S., Goto, S., Tsuji, H., Okuno, T., Asahara, T., Nomoto, K., Shibata, A., Fujisawa, Y., Minato, T., and Okamoto, A. (2015). Intestinal Dysbiosis and Lowered Serum Lipopolysaccharide-Binding Protein in Parkinson\u2019s Disease. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0142164"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.parkreldis.2016.08.019","article-title":"Short chain fatty acids and gut microbiota differ between patients with Parkinson\u2019s disease and age-matched controls","volume":"32","author":"Unger","year":"2016","journal-title":"Parkinsonism Relat. Disord."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1351","DOI":"10.1002\/mds.26307","article-title":"Colonic bacterial composition in Parkinson\u2019s disease","volume":"30","author":"Keshavarzian","year":"2015","journal-title":"Mov. Disord."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.brainres.2017.04.019","article-title":"Gut microbiota in Parkinson disease in a northern German cohort","volume":"1667","author":"Hopfner","year":"2017","journal-title":"Brain Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.cell.2016.01.013","article-title":"Are We Really Vastly Outnumbered? Revisiting the Ratio of Bacterial to Host Cells in Humans","volume":"164","author":"Sender","year":"2016","journal-title":"Cell"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"7297","DOI":"10.1007\/s12035-018-0937-8","article-title":"Bidirectional Neural Interaction Between Central Dopaminergic and Gut Lesions in Parkinson\u2019s Disease Models","volume":"55","author":"Guerra","year":"2018","journal-title":"Mol. Neurobiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nature08821","article-title":"A human gut microbial gene catalogue established by metagenomic sequencing","volume":"464","author":"Qin","year":"2010","journal-title":"Nature"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1007\/s00702-002-0808-2","article-title":"Idiopathic Parkinson\u2019s disease: Possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen","volume":"110","author":"Braak","year":"2003","journal-title":"J. Neural Transm. (Vienna)"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1002\/mds.25020","article-title":"Is alpha-synuclein in the colon a biomarker for premotor Parkinson\u2019s disease? Evidence from 3 cases","volume":"27","author":"Shannon","year":"2012","journal-title":"Mov. Disord. Off. J. Mov. Disord. Soc."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1002\/ana.24448","article-title":"Vagotomy and subsequent risk of Parkinson\u2019s disease","volume":"78","author":"Svensson","year":"2015","journal-title":"Ann. Neurol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1996","DOI":"10.1212\/WNL.0000000000003961","article-title":"Vagotomy and Parkinson disease: A Swedish register-based matched-cohort study","volume":"88","author":"Liu","year":"2017","journal-title":"Neurology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"574","DOI":"10.3389\/fneur.2019.00574","article-title":"The Gut and Parkinson\u2019s Disease-A Bidirectional Pathway","volume":"10","author":"Santos","year":"2019","journal-title":"Front. Neurol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"8546","DOI":"10.1523\/JNEUROSCI.5002-13.2014","article-title":"Neurodegeneration by activation of the microglial complement-phagosome pathway","volume":"34","author":"Bodea","year":"2014","journal-title":"J. Neurosci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"400","DOI":"10.4291\/wjgp.v5.i4.400","article-title":"Helicobacter pylori and neurological diseases: Married by the laws of inflammation","volume":"5","year":"2014","journal-title":"World J. Gastrointest. Pathophysiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1097\/MIB.0000000000000735","article-title":"Association Between Parkinson\u2019s Disease and Inflammatory Bowel Disease: A Nationwide Taiwanese Retrospective Cohort Study","volume":"22","author":"Lin","year":"2016","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/j.parkreldis.2018.02.022","article-title":"Fecal markers of intestinal inflammation and intestinal permeability are elevated in Parkinson\u2019s disease","volume":"50","author":"Schwiertz","year":"2018","journal-title":"Parkinsonism Relat. Disord."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"992","DOI":"10.3389\/fnins.2019.00992","article-title":"Fecal Calprotectin as a Marker of the Gut Immune System Activation Is Elevated in Parkinson\u2019s Disease","volume":"13","author":"Mulak","year":"2019","journal-title":"Front. Neurosci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1002\/mds.27326","article-title":"Stool Immune Profiles Evince Gastrointestinal Inflammation in Parkinson\u2019s Disease","volume":"33","author":"Houser","year":"2018","journal-title":"Mov. Disord."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.nbd.2012.09.007","article-title":"Colonic inflammation in Parkinson\u2019s disease","volume":"50","author":"Devos","year":"2013","journal-title":"Neurobiol. Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/s40478-015-0196-0","article-title":"Structural alterations of the intestinal epithelial barrier in Parkinson\u2019s disease","volume":"3","author":"Clairembault","year":"2015","journal-title":"Acta Neuropathol. Commun."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1586\/ern.11.192","article-title":"The management of gastrointestinal symptoms in Parkinson\u2019s disease","volume":"12","author":"Suchowersky","year":"2012","journal-title":"Expert Rev. Neurother."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Forsyth, C.B., Shannon, K.M., Kordower, J.H., Voigt, R.M., Shaikh, M., Jaglin, J.A., Estes, J.D., Dodiya, H.B., and Keshavarzian, A. (2011). Increased intestinal permeability correlates with sigmoid mucosa alpha-synuclein staining and endotoxin exposure markers in early Parkinson\u2019s disease. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0028032"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1002\/mds.26563","article-title":"Serum immune markers and disease progression in an incident Parkinson\u2019s disease cohort (ICICLE-PD)","volume":"31","author":"Wijeyekoon","year":"2016","journal-title":"Mov. Disord."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.neulet.2008.06.040","article-title":"Serum interleukin (IL-2, IL-10, IL-6, IL-4), TNFalpha and INFgamma concentrations are elevated in patients with atypical and idiopathic parkinsonism","volume":"441","author":"Brodacki","year":"2008","journal-title":"Neurosci. Lett."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1469","DOI":"10.1016\/j.cell.2016.11.018","article-title":"Gut Microbiota Regulate Motor Deficits and Neuroinflammation in a Model of Parkinson\u2019s Disease","volume":"167","author":"Sampson","year":"2016","journal-title":"Cell"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1038\/s41467-019-08294-y","article-title":"Gut bacterial tyrosine decarboxylases restrict levels of levodopa in the treatment of Parkinson\u2019s disease","volume":"10","author":"Frye","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Maini Rekdal, V., Bess, E.N., Bisanz, J.E., Turnbaugh, P.J., and Balskus, E.P. (2019). Discovery and inhibition of an interspecies gut bacterial pathway for Levodopa metabolism. Science, 364.","DOI":"10.1126\/science.aau6323"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"920","DOI":"10.3109\/00365529709011203","article-title":"Stool form scale as a useful guide to intestinal transit time","volume":"32","author":"Lewis","year":"1997","journal-title":"Scand. J. Gastroenterol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"867","DOI":"10.1002\/mds.10248","article-title":"Systematic evaluation of rating scales for impairment and disability in Parkinson\u2019s disease","volume":"17","author":"Ramaker","year":"2002","journal-title":"Mov. Disord."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"996","DOI":"10.1038\/nmeth.2604","article-title":"UPARSE: Highly accurate OTU sequences from microbial amplicon reads","volume":"10","author":"Edgar","year":"2013","journal-title":"Nat. Methods"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"7537","DOI":"10.1128\/AEM.01541-09","article-title":"Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities","volume":"75","author":"Schloss","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"D633","DOI":"10.1093\/nar\/gkt1244","article-title":"Ribosomal Database Project: Data and tools for high throughput rRNA analysis","volume":"42","author":"Cole","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2194","DOI":"10.1093\/bioinformatics\/btr381","article-title":"UCHIME improves sensitivity and speed of chimera detection","volume":"27","author":"Edgar","year":"2011","journal-title":"Bioinformatics"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"5261","DOI":"10.1128\/AEM.00062-07","article-title":"Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy","volume":"73","author":"Wang","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1007\/s13311-017-0598-8","article-title":"Microbiota Signaling Pathways that Influence Neurologic Disease","volume":"15","author":"Cox","year":"2018","journal-title":"Neurotherapeutics"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1038\/s41531-016-0002-0","article-title":"The gut-brain axis: Is intestinal inflammation a silent driver of Parkinson\u2019s disease pathogenesis?","volume":"3","author":"Houser","year":"2017","journal-title":"NPJ Parkinsons Dis."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Vital, M., Karch, A., and Pieper, D.H. (2017). Colonic Butyrate-Producing Communities in Humans: An Overview Using Omics Data. mSystems, 2.","DOI":"10.1128\/mSystems.00130-17"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"S70","DOI":"10.1177\/014860719902300518","article-title":"Physiological and anti-inflammatory roles of dietary fiber and butyrate in intestinal functions","volume":"23","author":"Andoh","year":"1999","journal-title":"JPEN J. Parenter Enteral Nutr."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"9351507","DOI":"10.1155\/2017\/9351507","article-title":"Proteobacteria: A Common Factor in Human Diseases","volume":"2017","author":"Rizzatti","year":"2017","journal-title":"Biomed. Res. Int."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Kim, S.J., Kim, S.E., Kim, A.R., Kang, S., Park, M.Y., and Sung, M.K. (2019). Dietary fat intake and age modulate the composition of the gut microbiota and colonic inflammation in C57BL\/6J mice. BMC Microbiol., 19.","DOI":"10.1186\/s12866-019-1557-9"},{"key":"ref_46","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_47","doi-asserted-by":"crossref","unstructured":"Pagliai, G., Russo, E., Niccolai, E., Dinu, M., Di Pilato, V., Magrini, A., Bartolucci, G., Baldi, S., Menicatti, M., and Giusti, B. (2019). Influence of a 3-month low-calorie Mediterranean diet compared to the vegetarian diet on human gut microbiota and SCFA: The CARDIVEG Study. Eur. J. Nutr.","DOI":"10.1017\/S0029665120001251"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"662","DOI":"10.1016\/j.chom.2015.03.005","article-title":"Crosstalk between Microbiota-Derived Short-Chain Fatty Acids and Intestinal Epithelial HIF Augments Tissue Barrier Function","volume":"17","author":"Kelly","year":"2015","journal-title":"Cell Host Microbe"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Gerhardt, S., and Mohajeri, M.H. (2018). Changes of Colonic Bacterial Composition in Parkinson\u2019s Disease and Other Neurodegenerative Diseases. Nutrients, 10.","DOI":"10.20944\/preprints201804.0370.v1"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1093\/aje\/kwh213","article-title":"Folate intake and risk of Parkinson\u2019s disease","volume":"160","author":"Chen","year":"2004","journal-title":"Am. J. Epidemiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1016\/0278-5846(94)90074-4","article-title":"Folic acid in neurodevelopment and child psychiatry","volume":"18","author":"Greenblatt","year":"1994","journal-title":"Prog. Neuropsychopharmacol. Biol. Psychiatry"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"4367","DOI":"10.1210\/jc.2016-1797","article-title":"Role of Gut Microbiota and Short Chain Fatty Acids in Modulating Energy Harvest and Fat Partitioning in Youth","volume":"101","author":"Goffredo","year":"2016","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1354","DOI":"10.3389\/fphar.2018.01354","article-title":"Gut Microbiota, Short-Chain Fatty Acids and Herbal Medicines","volume":"9","author":"Feng","year":"2018","journal-title":"Front. Pharmacol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1016\/j.tim.2016.09.011","article-title":"Rethinking Diet to Aid Human-Microbe Symbiosis","volume":"25","author":"Derrien","year":"2017","journal-title":"Trends Microbiol."},{"key":"ref_55","first-page":"200","article-title":"Impact of vegan diets on gut microbiota: An update on the clinical implications","volume":"30","author":"Wong","year":"2018","journal-title":"Ci Ji Yi Xue Za Zhi"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1038\/ismej.2012.104","article-title":"Gut microbiome composition is linked to whole grain-induced immunological improvements","volume":"7","author":"Lattimer","year":"2013","journal-title":"ISME J."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Klimenko, N.S., Tyakht, A.V., Popenko, A.S., Vasiliev, A.S., Altukhov, I.A., Ischenko, D.S., Shashkova, T.I., Efimova, D.A., Nikogosov, D.A., and Osipenko, D.A. (2018). Microbiome Responses to an Uncontrolled Short-Term Diet Intervention in the Frame of the Citizen Science Project. Nutrients, 10.","DOI":"10.3390\/nu10050576"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"E607","DOI":"10.1002\/oby.20466","article-title":"Human intestinal microbiota composition is associated with local and systemic inflammation in obesity","volume":"21","author":"Verdam","year":"2013","journal-title":"Obesity (Silver Spring)"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1186\/s12967-017-1175-y","article-title":"Influence of diet on the gut microbiome and implications for human health","volume":"15","author":"Singh","year":"2017","journal-title":"J. Transl. Med."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1519","DOI":"10.3748\/wjg.v17.i12.1519","article-title":"Potential beneficial effects of butyrate in intestinal and extraintestinal diseases","volume":"17","author":"Canani","year":"2011","journal-title":"World J. Gastroenterol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1016\/j.immuni.2015.09.007","article-title":"Dietary Fatty Acids Directly Impact Central Nervous System Autoimmunity via the Small Intestine","volume":"43","author":"Haghikia","year":"2015","journal-title":"Immunity"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1038\/nrmicro3344","article-title":"The gut microbiota, bacterial metabolites and colorectal cancer","volume":"12","author":"Louis","year":"2014","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1186\/s40168-018-0439-y","article-title":"Microbiome-host systems interactions: Protective effects of propionate upon the blood-brain barrier","volume":"6","author":"Hoyles","year":"2018","journal-title":"Microbiome"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"11312","DOI":"10.1074\/jbc.M211609200","article-title":"The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids","volume":"278","author":"Brown","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1038\/s41575-019-0157-3","article-title":"The role of short-chain fatty acids in microbiota-gut-brain communication","volume":"16","author":"Dalile","year":"2019","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1111\/imm.12645","article-title":"Communicating systems in the body: How microbiota and microglia cooperate","volume":"150","author":"Erny","year":"2017","journal-title":"Immunology"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1016\/j.neuint.2016.06.011","article-title":"The neuropharmacology of butyrate: The bread and butter of the microbiota-gut-brain axis?","volume":"99","author":"Stilling","year":"2016","journal-title":"Neurochem. Int."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1016\/j.foodchem.2012.06.013","article-title":"Changes in Maillard reaction products in ghee during storage","volume":"135","author":"Andrewes","year":"2012","journal-title":"Food Chem."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Gorkiewicz, G., Thallinger, G.G., Trajanoski, S., Lackner, S., Stocker, G., Hinterleitner, T., G\u00fclly, C., and H\u00f6genauer, C. (2013). Alterations in the colonic microbiota in response to osmotic diarrhea. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0055817"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"e143","DOI":"10.1038\/ctg.2015.54","article-title":"The Effects of Bowel Preparation on Microbiota-Related Metrics Differ in Health and in Inflammatory Bowel Disease and for the Mucosal and Luminal Microbiota Compartments","volume":"7","author":"Shobar","year":"2016","journal-title":"Clin. Transl. Gastroenterol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1097\/MEG.0000000000000581","article-title":"Persisting changes of intestinal microbiota after bowel lavage and colonoscopy","volume":"28","author":"Drago","year":"2016","journal-title":"Eur J. Gastroenterol. Hepatol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Harrell, L., Wang, Y., Antonopoulos, D., Young, V., Lichtenstein, L., Huang, Y., Hanauer, S., and Chang, E. (2012). Standard colonic lavage alters the natural state of mucosal-associated microbiota in the human colon. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0032545"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"4042","DOI":"10.1038\/s41598-019-40182-9","article-title":"Effects of bowel preparation on the human gut microbiome and metabolome","volume":"9","author":"Nagata","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Reese, A.T., and Dunn, R.R. (2018). Drivers of Microbiome Biodiversity: A Review of General Rules, Feces and Ignorance. MBio, 9.","DOI":"10.1128\/mBio.01294-18"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/s00702-015-1463-8","article-title":"Therapy-resistant symptoms in Parkinson\u2019s disease","volume":"123","author":"Vorovenci","year":"2016","journal-title":"J. Neural Transm. (Vienna)"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1602","DOI":"10.1002\/mds.26712","article-title":"Unmasking levodopa resistance in Parkinson\u2019s disease","volume":"31","author":"Nonnekes","year":"2016","journal-title":"Mov. Disord."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"e3019","DOI":"10.7717\/peerj.3019","article-title":"Key bacterial families (Clostridiaceae, Erysipelotrichaceae and Bacteroidaceae) are related to the digestion of protein and energy in dogs","volume":"5","author":"Bermingham","year":"2017","journal-title":"PeerJ"},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Odamaki, T., Kato, K., Sugahara, H., Hashikura, N., Takahashi, S., Xiao, J.Z., Abe, F., and Osawa, R. (2016). Age-related changes in gut microbiota composition from newborn to centenarian: A cross-sectional study. BMC Microbiol., 16.","DOI":"10.1186\/s12866-016-0708-5"}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/9\/2\/376\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T08:55:21Z","timestamp":1760172921000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/9\/2\/376"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,6]]},"references-count":78,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2020,2]]}},"alternative-id":["cells9020376"],"URL":"https:\/\/doi.org\/10.3390\/cells9020376","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,2,6]]}}}