{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,19]],"date-time":"2026-08-19T18:55:51Z","timestamp":1787165751901,"version":"build-2736575974"},"reference-count":38,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,10,6]],"date-time":"2022-10-06T00:00:00Z","timestamp":1665014400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:sec>\n                    <jats:title>Objective<\/jats:title>\n                    <jats:p>To explore the effect of probiotics combined with prebiotics on clinical hypothyroidism during pregnancy combined with small intestinal bacterial overgrowth.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>(1) In total, 441 pregnant women were included in this study. A total of 231 patients with clinical hypothyroidism during the second trimester of pregnancy and 210 normal pregnant women were enrolled in the lactulose methane-hydrogen breath test. The positive rate of intestinal bacterial overgrowth (SIBO), gastrointestinal symptoms, thyroid function and inflammatory factors were compared between the two groups by chi-square test and two independent sample t-test. (2) SIBO-positive patients in the clinical hypothyroidism group during pregnancy (n=112) were treated with probiotics combined with prebiotics based on conventional levothyroxine sodium tablets treatment. The changes in the methane-hydrogen breath test, gastrointestinal symptoms, thyroid function and inflammatory factors were compared before treatment (G0) and 21 days after treatment (G21) by chi-square test and paired sample t test.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>(1) The positive rates of SIBO in pregnant women in the clinical hypothyroidism group and control group were 48.5% and 24.8%, respectively. (2) The incidence of abdominal distention and constipation in the clinical hypothyroidism group was significantly higher than that in the control group, and the risk of abdominal distention and constipation in SIBO-positive pregnant women was higher than that in SIBO-negative pregnant women. (3) The serum levels of hypersensitive C-reactive protein (hsCRP), IL-10, IL-6, TNF-\u03b1, low-density lipoprotein (LDL), total cholesterol (TC), free fatty acids (FFAs) and apolipoprotein B (ApoB) in the hypothyroidism group during pregnancy were higher than those in the control group. (4) After 21 days of probiotics combined with prebiotics, the incidence of pure methane positivity in the methane-hydrogen breath test in the G21 group was significantly reduced, and the average abundance of hydrogen and methane at each time point in the G21 group was lower than that in the G0 group. (5) The incidence of constipation in the G21 group was significantly lower than before treatment. (6) The levels of serum TSH, hsCRP, IL-6, TNF-\u03b1, TC and LDL in pregnant women after probiotics combined with prebiotics were lower than those before treatment.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>Probiotics combined with prebiotics are effective in the treatment of pregnant patients with clinical hypothyroidism complicated with SIBO, providing a new idea to treat pregnant patients with clinical hypothyroidism complicated with SIBO.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.3389\/fcimb.2022.983027","type":"journal-article","created":{"date-parts":[[2022,10,6]],"date-time":"2022-10-06T11:22:14Z","timestamp":1665055334000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":15,"title":["Efficacy evaluation of probiotics combined with prebiotics in patients with clinical hypothyroidism complicated with small intestinal bacterial overgrowth during the second trimester of pregnancy"],"prefix":"10.3389","volume":"12","author":[{"given":"Yingqi","family":"Hao","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yajuan","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanjie","family":"Ban","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingjing","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bo","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian","family":"Ouyang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zongzong","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miao","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanjun","family":"Cai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mengqi","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wentao","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,10,6]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"426","DOI":"10.1139\/cjpp-2015-0247","article-title":"Effect of magnesium sulfate and thyroxine on inflammatory markers in a rat model of hypothyroidism","volume":"94","author":"Abbas","year":"2016","journal-title":"Can. J. Physiol. Pharmacol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"627","DOI":"10.2147\/IMCRJ.S326481","article-title":"Levothyroxine sodium oral solution normalizes thyroid function in a patient with hashimoto\u2019s disease, gastritis, diabetic gastroparesis, and small intestinal bacterial overgrowth (SIBO)","volume":"14","author":"Bohinc Henderson","year":"2021","journal-title":"Int. Med. Case Rep. J."},{"key":"B3","doi-asserted-by":"publisher","first-page":"e261","DOI":"10.1097\/AOG.0000000000003893","article-title":"Thyroid disease in pregnancy: ACOG practice bulletin, number 223","volume":"135","author":"Casey","year":"2020","journal-title":"Obstet. gynecol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1097\/MCG.0b013e3181d6bc3e","article-title":"The thyroid and the gut","volume":"44","author":"Ebert","year":"2010","journal-title":"J. Clin. gastroenterol0"},{"key":"B5","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1007\/s13311-017-0600-5","article-title":"Gut microbiota and the neuroendocrine system","volume":"15","author":"Farzi","year":"2018","journal-title":"Neurotherapeutics: J. Am. Soc. Exp. NeuroTherapeutics."},{"key":"B6","doi-asserted-by":"publisher","first-page":"01","DOI":"10.1210\/clinem\/dgaa555","article-title":"Maternal thyroid dysfunction during pregnancy and the risk of adverse outcomes in the offspring","volume":"12","author":"Ge","year":"2020","journal-title":"A Syst. Rev. Meta-Analysis 2020"},{"key":"B7","doi-asserted-by":"publisher","first-page":"1189","DOI":"10.1111\/j.1440-1746.2010.06353.x","article-title":"Asian Consensus on irritable bowel syndrome","volume":"25","author":"Gwee","year":"2010","journal-title":"J. Gastroenterol. hepatol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"266","DOI":"10.4236\/aim.2016.64028","article-title":"Synbiotic as feed additives relating to animal health and performance","volume":"6","author":"Hamasalim","year":"2016","journal-title":"Adv. Microbiol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1080\/00325481.2018.11704724","article-title":"Constipation: Evaluation and management","volume":"115","author":"Jani","year":"2018","journal-title":"Missouri Med."},{"key":"B10","doi-asserted-by":"publisher","first-page":"1347","DOI":"10.1016\/j.jacl.2017.08.015","article-title":"Association between thyroid function and lipid profiles, apolipoproteins, and high-density lipoprotein function","volume":"11","author":"Jung","year":"2017","journal-title":"J. Clin. lipidol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"82.e1","DOI":"10.1016\/j.ajog.2020.06.052","article-title":"Prevalence of inadequate and excessive iodine intake in a US pregnancy cohort","volume":"224","author":"Kerver","year":"2021","journal-title":"Am. J. obstet. gynecol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"1769","DOI":"10.3390\/nu12061769","article-title":"Thyroid-Gut-Axis","volume":"12","author":"Knezevic","year":"2020","journal-title":"How Does Microbiota Influence Thyroid Function?"},{"key":"B13","doi-asserted-by":"publisher","first-page":"4180","DOI":"10.1210\/jc.2007-0606","article-title":"Association between hypothyroidism and small intestinal bacterial overgrowth","volume":"92","author":"Lauritano","year":"2007","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"B14","doi-asserted-by":"publisher","first-page":"6176","DOI":"10.1073\/pnas.0308766101","article-title":"Methanogenic archaea and human periodontal disease","volume":"101","author":"Lepp","year":"2004","journal-title":"Proc. Natl. Acad. Sci. United States America."},{"key":"B15","doi-asserted-by":"publisher","first-page":"19689","DOI":"10.1038\/s41598-021-99252-6","article-title":"Differential lipids in pregnant women with subclinical hypothyroidism and their correlation to the pregnancy outcomes","volume":"11","author":"Li","year":"2021","journal-title":"Sci. Rep."},{"key":"B16","doi-asserted-by":"publisher","first-page":"478","DOI":"10.3390\/nu9091021","article-title":"Effects of probiotics, prebiotics, and synbiotics on human health","volume":"9","author":"Markowiak","year":"2017","journal-title":"Nutrients"},{"key":"B17","doi-asserted-by":"publisher","first-page":"930","DOI":"10.3945\/ajcn.117.156265","article-title":"Short-chain fatty acids, prebiotics, synbiotics, and systemic inflammation: a systematic review and meta-analysis","volume":"106","author":"McLoughlin","year":"2017","journal-title":"Am. J. Clin. Nutr."},{"key":"B18","doi-asserted-by":"publisher","first-page":"429","DOI":"10.17306\/j.Afs.0953","article-title":"Characterization of stirred yoghurt enriched with probiotics and beetroot and its therapeutic potential in experimental type 2 diabetes","volume":"20","author":"Mohamed","year":"2021","journal-title":"Acta scientiarum polonorum Technologia. alimentaria."},{"key":"B19","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1089\/acm.2020.0275","article-title":"Alternative treatment approaches to small intestinal bacterial overgrowth: A systematic review","volume":"27","author":"Nickles","year":"2021","journal-title":"J. Altern. complementary Med. (New York NY)."},{"key":"B20","doi-asserted-by":"publisher","first-page":"575840","DOI":"10.1155\/2011\/575840","article-title":"Lipid abnormalities and cardiometabolic risk in patients with overt and subclinical thyroid disease","volume":"2011","author":"Peppa","year":"2011","journal-title":"J. lipids."},{"key":"B21","doi-asserted-by":"publisher","first-page":"1297","DOI":"10.1007\/s10620-006-9104-6","article-title":"Neomycin improves constipation-predominant irritable bowel syndrome in a fashion that is dependent on the presence of methane gas: subanalysis of a double-blind randomized controlled study","volume":"51","author":"Pimentel","year":"2006","journal-title":"Digestive Dis. Sci."},{"key":"B22","doi-asserted-by":"publisher","first-page":"165","DOI":"10.14309\/ajg.0000000000000501","article-title":"ACG clinical guideline: Small intestinal bacterial overgrowth","volume":"115","author":"Pimentel","year":"2020","journal-title":"Am. J. gastroenterol0"},{"key":"B23","doi-asserted-by":"publisher","first-page":"775","DOI":"10.1038\/ajg.2017.46","article-title":"Hydrogen and methane-based breath testing in gastrointestinal disorders: The north American consensus","volume":"112","author":"Rezaie","year":"2017","journal-title":"Am. J. gastroenterol0"},{"key":"B24","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1016\/j.cgh.2016.07.028","article-title":"Chronic diarrhea: Diagnosis and management","volume":"15","author":"Schiller","year":"2017","journal-title":"Clin. Gastroenterol. hepatology: Off. Clin. Pract. J. Am. Gastroenterol. Assoc."},{"key":"B25","doi-asserted-by":"publisher","first-page":"1071","DOI":"10.1111\/j.1365-2036.2011.04637.x","article-title":"Review article: the treatment of functional abdominal bloating and distension","volume":"33","author":"Schmulson","year":"2011","journal-title":"Alimentary Pharmacol. Ther."},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.3390\/nu12010222","article-title":"Effects of synbiotic supplement on human gut microbiota, body composition and weight loss in obesity","volume":"12","author":"Sergeev","year":"2020","journal-title":"Nutrients"},{"key":"B27","doi-asserted-by":"publisher","first-page":"1524","DOI":"10.1007\/s10620-010-1447-3","article-title":"Small intestinal bacterial overgrowth in nonalcoholic steatohepatitis: association with toll-like receptor 4 expression and plasma levels of interleukin 8","volume":"56","author":"Shanab","year":"2011","journal-title":"Digestive Dis. Sci."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1521","DOI":"10.1042\/CS20200475","article-title":"Gut dysbiosis is associated with primary hypothyroidism with interaction on gut-thyroid axis","volume":"134","author":"Su","year":"2020","journal-title":"Clin. Sci. (Lond)."},{"key":"B29","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1186\/s13068-018-1237-2","article-title":"The diversity of hydrogen-producing bacteria and methanogens within an in situ coal seam","volume":"11","author":"Su","year":"2018","journal-title":"Biotechnol. biofuels."},{"key":"B30","doi-asserted-by":"publisher","first-page":"102234","DOI":"10.1016\/j.ctim.2019.102234","article-title":"The effects of synbiotic supplementation on thyroid function and inflammation in hypothyroid patients: A randomized, double\u2212blind, placebo\u2212controlled trial","volume":"48","author":"Talebi","year":"2020","journal-title":"Complementary therapies Med."},{"key":"B31","doi-asserted-by":"publisher","first-page":"965","DOI":"10.1530\/EC-21-0212","article-title":"C-reactive protein and thyroid-stimulating hormone levels as risk factors for hypothyroidism in patients with subacute thyroiditis","volume":"10","author":"Tang","year":"2021","journal-title":"Endocr. connections"},{"key":"B32","doi-asserted-by":"publisher","first-page":"3092","DOI":"10.1039\/C8FO00157J","article-title":"Barley \u03b2-glucan increases fecal bile acid excretion and short chain fatty acid levels in mildly hypercholesterolemic individuals","volume":"9","author":"Thandapilly","year":"2018","journal-title":"Food Funct."},{"key":"B33","doi-asserted-by":"publisher","first-page":"858","DOI":"10.3390\/nu3100858","article-title":"Regulation of inflammation by short chain fatty acids","volume":"3","author":"Vinolo","year":"2011","journal-title":"Nutrients"},{"key":"B34","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1007\/s12020-014-0509-2","article-title":"Does microbiota composition affect thyroid homeostasis","volume":"49","author":"Virili","year":"2015","journal-title":"Endocrine"},{"key":"B35","doi-asserted-by":"publisher","first-page":"3970","DOI":"10.3748\/wjg.v16.i31.3970","article-title":"Use of pre-, pro- and synbiotics in patients with acute pancreatitis: a meta-analysis","volume":"16","author":"Zhang","year":"2010","journal-title":"World J. gastroenterol0"},{"key":"B36","doi-asserted-by":"publisher","first-page":"564","DOI":"10.1007\/s12020-018-1831-x","article-title":"Dysbiosis of the gut microbiome is associated with thyroid cancer and thyroid nodules and correlated with clinical index of thyroid function","volume":"64","author":"Zhang","year":"2019","journal-title":"Endocrine"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.3389\/fendo.2021.796212","article-title":"Elevated levels of circulating biomarkers related to leaky gut syndrome and bacterial translocation are associated with graves\u2019 disease","volume":"12","author":"Zheng","year":"2021","journal-title":"Front. endocrinol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"408","DOI":"10.1097\/MED.0b013e32833d6d46","article-title":"New insights into regulation of lipid metabolism by thyroid hormone","volume":"17","author":"Zhu","year":"2010","journal-title":"Curr. Opin. endocrinol. diabetes Obes."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2022.983027\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,6]],"date-time":"2022-10-06T11:22:17Z","timestamp":1665055337000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2022.983027\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,6]]},"references-count":38,"alternative-id":["10.3389\/fcimb.2022.983027"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2022.983027","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,6]]},"article-number":"983027"}}