{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T05:34:02Z","timestamp":1792647242323,"version":"4.5.0"},"reference-count":33,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2020,8,17]],"date-time":"2020-08-17T00:00:00Z","timestamp":1597622400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Science and Technology (Taiwan)","award":["MOST 106-2320-B-039-044-MY3"],"award-info":[{"award-number":["MOST 106-2320-B-039-044-MY3"]}]},{"DOI":"10.13039\/501100007300","name":"China Medical University","doi-asserted-by":"publisher","award":["CMU108-ASIA-03"],"award-info":[{"award-number":["CMU108-ASIA-03"]}],"id":[{"id":"10.13039\/501100007300","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>Chronic inflammation caused by Helicobacter pylori infection increases the risk of developing gastric cancer. Even though the prevalence of H. pylori infection has been decreased in many regions, the development of antibiotic resistance strains has increased the difficulty of eradicating H. pylori. Therefore, exploring alternative approaches to combat H. pylori infection is required. It is well-known that probiotic therapy can improve H. pylori clearance. In this study, H. pylori-infected mice were treated with Lactobacillus fermentum P2 (P2), L. casei L21 (L21), L. rhamnosus JB3 (JB3), or a mixture including the aforementioned three (multi-LAB) for three days. All the lactic acid producing bacteria (LAB) treatments decreased H. pylori loads in the stomach and vacA gene expression, H. pylori specific immunoglobulin (Ig) A, and IgM levels in stomach homogenates, as well as serum levels of interferon-gamma and interleukin-1 beta. The multi-LAB and JB3 treatments further restored the superoxide dismutase and catalase activities suppressed by H. pylori infection. Furthermore, H. pylori infection decreased serum concentrations of 15 kinds of amino acids as well as palmitic acid. The multi-LAB treatment was able to recover the serum levels of alanine, arginine, aspartate, glycine, and tryptophan, which are all important in modulating immune functions. In addition, butyric acid, valeric acid, palmitic acid, palmitoleic acid, stearic acid, and oleic acid levels were increased. In this study, multi-LAB revealed its ability to adjust the composition of metabolites to improve health. To date, the mechanisms underlying how LAB strains crosstalk with the host are not fully understood. Identifying the mechanisms which are regulated by LABs will facilitate the development of effective therapies for infection in the future.<\/jats:p>","DOI":"10.3390\/nu12082476","type":"journal-article","created":{"date-parts":[[2020,8,17]],"date-time":"2020-08-17T21:58:53Z","timestamp":1597701533000},"page":"2476","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":40,"title":["Effects of Multi-Strain Probiotics on Immune Responses and Metabolic Balance in Helicobacter pylori-Infected Mice"],"prefix":"10.3390","volume":"12","author":[{"given":"Chun-Che","family":"Lin","sequence":"first","affiliation":[{"name":"Department of Internal Medicine, China Medical University Hospital, China Medical University, Taichung 404333, Taiwan"},{"name":"School of Medicine, China Medical University, Taichung 404333, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei-Chiao","family":"Huang","sequence":"additional","affiliation":[{"name":"Department of Nutrition, China Medical University, Taichung 404333, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiu-Hsian","family":"Su","sequence":"additional","affiliation":[{"name":"Department of Biological Science and Technology, China Medical University, Taichung 404333, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei-De","family":"Lin","sequence":"additional","affiliation":[{"name":"Department of Medical Research, China Medical University Hospital, China Medical University, Taichung 404333, Taiwan"},{"name":"School of Post Baccalaureate Chinese Medicine, China Medical University, Taichung 404333, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Tzu","family":"Wu","sequence":"additional","affiliation":[{"name":"Department of Health and Nutrition Biotechnology, Asia University, Taichung 413305, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bi","family":"Yu","sequence":"additional","affiliation":[{"name":"Department of Animal Science, College of Agriculture and Natural Resources, National Chung Hsing University, Taichung 402204, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4575-7475","authenticated-orcid":false,"given":"Yuan-Man","family":"Hsu","sequence":"additional","affiliation":[{"name":"Department of Biological Science and Technology, China Medical University, Taichung 404333, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,8,17]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"e12514","DOI":"10.1111\/hel.12514","article-title":"Epidemiology of Helicobacter pylori infection","volume":"23","author":"Sjomina","year":"2018","journal-title":"Helicobacter"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e12635","DOI":"10.1111\/hel.12635","article-title":"Review: Epidemiology of Helicobacter pylori infection","volume":"24","author":"Leja","year":"2019","journal-title":"Helicobacter"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1128\/CMR.00011-10","article-title":"Helicobacter pylori and gastric cancer: Factors that modulate disease risk","volume":"23","author":"Wroblewski","year":"2010","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_4","first-page":"351","article-title":"Update on Helicobacter pylori treatment","volume":"75","author":"Ables","year":"2007","journal-title":"Am. Fam. Physician"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1097\/QCO.0000000000000396","article-title":"Antibiotic resistance in Helicobacter pylori","volume":"30","author":"Alba","year":"2017","journal-title":"Curr. Opin. Infect. Dis."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00253-017-8535-7","article-title":"Helicobacter pylori treatment: Antibiotics or probiotics","volume":"102","author":"Goderska","year":"2018","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1159\/000007660","article-title":"Effect of whey-based culture supernatant of Lactobacillus acidophilus (johnsonii) La1 on Helicobacter pylori infection in humans","volume":"60","author":"Michetti","year":"1999","journal-title":"Digestion"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"3118","DOI":"10.1111\/1750-3841.14372","article-title":"Baicalin, Baicalein, and Lactobacillus Rhamnosus JB3 Alleviated Helicobacter pylori infections in vitro and in vivo","volume":"83","author":"Chen","year":"2018","journal-title":"J. Food Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1046\/j.1365-2036.2003.01675.x","article-title":"Favourable effect of regular intake of fermented milk containing Lactobacillus johnsonii on Helicobacter pylori associated gastritis","volume":"18","author":"Pantoflickova","year":"2003","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"319","DOI":"10.3389\/fimmu.2018.00319","article-title":"Amino acids as mediators of metabolic cross talk between host and pathogen","volume":"9","author":"Ren","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/j.anaerobe.2007.04.006","article-title":"Different probiotic properties for Lactobacillus fermentum strains isolated from swine and poultry","volume":"13","author":"Lin","year":"2007","journal-title":"Anaerobe"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"32","DOI":"10.2141\/jpsa.0170179","article-title":"Effects of multi-strain probiotics combined with gardeniae fructus on intestinal microbiota, metabolites, and morphology in broilers","volume":"56","author":"Chang","year":"2019","journal-title":"J. Poult. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2\u2212\u0394\u0394CT Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1502","DOI":"10.1111\/j.1572-0241.1999.01133.x","article-title":"Genotypes of Helicobacter pylori obtained from gastric ulcer patients taking or not taking NSAIDs","volume":"94","author":"Li","year":"1999","journal-title":"Am. J. Gastroenterol."},{"key":"ref_15","first-page":"224","article-title":"A pilot study of neonatal screening by electrospray ionization tandem mass spectrometry in Taiwan","volume":"42","author":"Lin","year":"2001","journal-title":"Acta Paediatr. Taiwan"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1203\/00006450-199509000-00009","article-title":"Diagnosis of inborn errors of metabolism from blood spots by acylcarnitines and amino acids profiling using automated electrospray tandem mass spectrometry","volume":"38","author":"Rashed","year":"1995","journal-title":"Pediatr. Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1038\/nrmicro1095","article-title":"Helicobacter pylori VacA, a paradigm for toxin multifunctionality","volume":"3","author":"Cover","year":"2005","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1016\/j.micpath.2018.10.012","article-title":"Inflammasome activation and regulation during Helicobacter pylori pathogenesis","volume":"125","author":"Kumar","year":"2018","journal-title":"Microb. Pathog."},{"key":"ref_19","first-page":"129","article-title":"The requirements of protein & amino acid during acute & chronic infections","volume":"124","author":"Kurpad","year":"2006","journal-title":"Indian J. Med. Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"789","DOI":"10.3904\/kjim.2015.30.6.789","article-title":"Time to learn from the past and prepare for the future in Helicobacter pylori eradication","volume":"30","author":"Bang","year":"2015","journal-title":"Korean J. Intern. Med."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1007\/s00228-017-2291-6","article-title":"Efficacy and safety of probiotic-supplemented triple therapy for eradication of Helicobacter pylori in children: A systematic review and network meta-analysis","volume":"73","author":"Feng","year":"2017","journal-title":"Eur. J. Clin. Pharmacol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"988","DOI":"10.3945\/jn.114.192120","article-title":"Dietary arginine supplementation of mice alters the microbial population and activates intestinal innate immunity","volume":"144","author":"Ren","year":"2014","journal-title":"J. Nutr."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1189\/jlb.4A0615-252R","article-title":"Asparagine deprivation mediated by Salmonella asparaginase causes suppression of activation-induced T cell metabolic reprogramming","volume":"99","author":"Torres","year":"2016","journal-title":"J. Leukoc. Biol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"8841","DOI":"10.1073\/pnas.97.16.8841","article-title":"Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens","volume":"97","author":"Nathan","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1017\/S000711450769936X","article-title":"Amino acids and immune function","volume":"98","author":"Li","year":"2007","journal-title":"Br. J. Nutr."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2023","DOI":"10.1099\/mic.0.26203-0","article-title":"L-Serine, D- and L-proline and alanine as respiratory substrates of Helicobacter pylori: Correlation between in vitro and in vivo amino acid levels","volume":"149","author":"Nagata","year":"2003","journal-title":"Microbiology"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"30","DOI":"10.3904\/kjim.2016.31.1.30","article-title":"The antibacterial effect of fatty acids on Helicobacter pylori infection","volume":"31","author":"Jung","year":"2016","journal-title":"Korean J. Intern. Med."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1099\/00222615-42-4-276","article-title":"The effects of unsaturated fatty acids on Helicobacter pylori in vitro","volume":"42","author":"Khulusi","year":"1995","journal-title":"J. Med. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/S0928-8244(03)00008-7","article-title":"Antibacterial actions of fatty acids and monoglycerides against Helicobacter pylori","volume":"36","author":"Sun","year":"2003","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1007\/s11883-010-0131-6","article-title":"Saturated fatty acids and risk of coronary heart disease: Modulation by replacement nutrients","volume":"12","author":"Sun","year":"2010","journal-title":"Curr. Atheroscler. Rep."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"3129","DOI":"10.1038\/s41467-018-05614-6","article-title":"Dietary stearic acid regulates mitochondria in vivo in humans","volume":"9","author":"Pfaff","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1016\/j.tem.2017.11.009","article-title":"Palmitic and oleic acid: The yin and yang of fatty acids in Type 2 Diabetes Mellitus","volume":"29","author":"Palomer","year":"2018","journal-title":"Trends Endocrinol. Metab."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1111\/j.1440-1746.2006.04213.x","article-title":"Does butyrate protect from colorectal cancer?","volume":"21","author":"Sengupta","year":"2006","journal-title":"J. Gastroenterol. Hepatol."}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/12\/8\/2476\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:02:06Z","timestamp":1760176926000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/12\/8\/2476"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,8,17]]},"references-count":33,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2020,8]]}},"alternative-id":["nu12082476"],"URL":"https:\/\/doi.org\/10.3390\/nu12082476","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,8,17]]}}}