{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,12]],"date-time":"2026-04-12T19:52:22Z","timestamp":1776023542893,"version":"3.50.1"},"reference-count":34,"publisher":"Springer Science and Business Media LLC","issue":"12","license":[{"start":{"date-parts":[[2018,9,20]],"date-time":"2018-09-20T00:00:00Z","timestamp":1537401600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"funder":[{"DOI":"10.13039\/501100002341","name":"Academy of Finland","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100002341","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006306","name":"Sigrid Jus\u00e9liuksen S\u00e4\u00e4ti\u00f6","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100006306","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004212","name":"P\u00e4ivikki ja Sakari Sohlbergin S\u00e4\u00e4ti\u00f6","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004212","id-type":"DOI","asserted-by":"publisher"}]},{"name":"the Competitive State Research Financing of the Expert Area of Tampere University Hospital"},{"DOI":"10.13039\/501100005744","name":"Lastentautien Tutkimuss\u00e4\u00e4ti\u00f6","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100005744","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010114","name":"Yrj\u00f6 Jahnssonin S\u00e4\u00e4ti\u00f6","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100010114","id-type":"DOI","asserted-by":"publisher"}]},{"name":"State Fund","award":["Y1023G2017"],"award-info":[{"award-number":["Y1023G2017"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Dig Dis Sci"],"published-print":{"date-parts":[[2018,12]]},"DOI":"10.1007\/s10620-018-5285-z","type":"journal-article","created":{"date-parts":[[2018,9,20]],"date-time":"2018-09-20T11:44:07Z","timestamp":1537443847000},"page":"3434-3441","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Microbial Biomarkers in Patients with Nonresponsive Celiac Disease"],"prefix":"10.1007","volume":"63","author":[{"given":"Liisa","family":"Viitasalo","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4757-2164","authenticated-orcid":false,"given":"Kalle","family":"Kurppa","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Merja","family":"Ashorn","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"P\u00e4ivi","family":"Saavalainen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Heini","family":"Huhtala","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sara","family":"Ashorn","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Markku","family":"M\u00e4ki","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tuire","family":"Ilus","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Katri","family":"Kaukinen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sari","family":"Iltanen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2018,9,20]]},"reference":[{"key":"5285_CR1","doi-asserted-by":"publisher","first-page":"2016","DOI":"10.1111\/j.1572-0241.2002.05917.x","volume":"97","author":"AS Abdulkarim","year":"2002","unstructured":"Abdulkarim AS, Burgart LJ, See J, Murray JA. Etiology of nonresponsive celiac disease: results of a systematic approach. Am J Gastroenterol. 2002;97:2016\u20132021.","journal-title":"Am J Gastroenterol"},{"key":"5285_CR2","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1016\/j.cgh.2006.12.006","volume":"5","author":"DA Leffler","year":"2007","unstructured":"Leffler DA, Dennis M, Hyett B, Kelly E, Schuppan D, Kelly CP. Etiologies and predictors of diagnosis in nonresponsive celiac disease. Clin Gastroenterol Hepatol. 2007;5:445\u2013450.","journal-title":"Clin Gastroenterol Hepatol"},{"key":"5285_CR3","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1097\/MCG.0000000000000392","volume":"50","author":"E Stasi","year":"2016","unstructured":"Stasi E, Marafini I, Caruso R, et al. Frequency and cause of persistent symptoms in celiac disease patients on a long-term gluten-free diet. J Clin Gastroenterol. 2016;50:239\u2013243.","journal-title":"J Clin Gastroenterol"},{"key":"5285_CR4","doi-asserted-by":"publisher","first-page":"418","DOI":"10.1111\/apt.12606","volume":"39","author":"T Ilus","year":"2014","unstructured":"Ilus T, Kaukinen K, Virta LJ, et al. Refractory coeliac disease in a country with a high prevalence of clinically-diagnosed coeliac disease. Aliment Pharmacol Ther. 2014;39:418\u2013425.","journal-title":"Aliment Pharmacol Ther"},{"key":"5285_CR5","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1186\/1471-2180-10-63","volume":"10","author":"G Palma De","year":"2010","unstructured":"De Palma G, Nadal I, Medina M, et al. Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol. 2010;10:63.","journal-title":"BMC Microbiol"},{"key":"5285_CR6","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1053\/j.gastro.2016.10.012","volume":"152","author":"RB Sartor","year":"2017","unstructured":"Sartor RB, Wu GD. Roles for intestinal bacteria, viruses, and fungi in pathogenesis of inflammatory bowel diseases and therapeutic approaches. Gastroenterology. 2017;152:327.","journal-title":"Gastroenterology"},{"key":"5285_CR7","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1097\/01.MIB.0000218765.84087.42","volume":"12","author":"S Iltanen","year":"2006","unstructured":"Iltanen S, Tervo L, Halttunen T, et al. Elevated serum anti-I2 and anti-OmpW antibody levels in children with IBD. Inflamm Bowel Dis. 2006;12:389\u2013394.","journal-title":"Inflamm Bowel Dis"},{"key":"5285_CR8","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1002\/ibd.20535","volume":"15","author":"S Ashorn","year":"2009","unstructured":"Ashorn S, Honkanen T, Kolho KL, et al. Fecal calprotectin levels and serological responses to microbial antigens among children and adolescents with inflammatory bowel disease. Inflamm Bowel Dis. 2009;15:199\u2013205.","journal-title":"Inflamm Bowel Dis"},{"key":"5285_CR9","doi-asserted-by":"publisher","first-page":"689","DOI":"10.1053\/gast.2002.35379","volume":"123","author":"CJ Landers","year":"2002","unstructured":"Landers CJ, Cohavy O, Misra R, et al. Selected loss of tolerance evidenced by Crohn\u2019s disease-associated immune responses to auto- and microbial antigens. Gastroenterology. 2002;123:689\u2013699.","journal-title":"Gastroenterology"},{"key":"5285_CR10","doi-asserted-by":"publisher","first-page":"1933","DOI":"10.1038\/ajg.2014.355","volume":"109","author":"P Wacklin","year":"2014","unstructured":"Wacklin P, Laurikka P, Lindfors K, et al. Altered duodenal microbiota composition in celiac disease patients suffering from persistent symptoms on a long-term gluten-free diet. Am J Gastroenterol. 2014;109:1933\u20131941.","journal-title":"Am J Gastroenterol"},{"key":"5285_CR11","doi-asserted-by":"publisher","first-page":"1117","DOI":"10.1136\/gut.2003.030734","volume":"53","author":"DG Forcione","year":"2004","unstructured":"Forcione DG, Rosen MJ, Kisiel JB, Sands BE. Anti-Saccharomyces cerevisiae antibody (ASCA) positivity is associated with increased risk for early surgery in Crohn\u2019s disease. Gut. 2004;53:1117\u20131122.","journal-title":"Gut"},{"key":"5285_CR12","doi-asserted-by":"publisher","first-page":"665","DOI":"10.1111\/j.1572-0241.2007.01652.x","volume":"103","author":"M Papp","year":"2008","unstructured":"Papp M, Altorjay I, Dotan N, et al. New serological markers for inflammatory bowel disease are associated with earlier age at onset, complicated disease behavior, risk for surgery, and NOD2\/CARD15 genotype in a Hungarian IBD cohort. Am J Gastroenterol. 2008;103:665\u2013681.","journal-title":"Am J Gastroenterol"},{"key":"5285_CR13","doi-asserted-by":"publisher","first-page":"2376","DOI":"10.1111\/j.1572-0241.2004.40417.x","volume":"99","author":"ID Arnott","year":"2004","unstructured":"Arnott ID, Landers CJ, Nimmo EJ, et al. Sero-reactivity to microbial components in Crohn\u2019s disease is associated with disease severity and progression, but not NOD2\/CARD15 genotype. Am J Gastroenterol. 2004;99:2376\u20132384.","journal-title":"Am J Gastroenterol"},{"key":"5285_CR14","doi-asserted-by":"publisher","first-page":"414","DOI":"10.1053\/j.gastro.2003.11.015","volume":"126","author":"WS Mow","year":"2004","unstructured":"Mow WS, Vasiliauskas EA, Lin YC, et al. Association of antibody responses to microbial antigens and complications of small bowel Crohn\u2019s disease. Gastroenterology. 2004;126:414\u2013424.","journal-title":"Gastroenterology"},{"key":"5285_CR15","doi-asserted-by":"publisher","first-page":"881","DOI":"10.1111\/j.1365-2036.2005.02417.x","volume":"21","author":"A Granito","year":"2005","unstructured":"Granito A, Zauli D, Muratori P, et al. Anti-Saccharomyces cerevisiae and perinuclear anti-neutrophil cytoplasmic antibodies in coeliac disease before and after gluten-free diet. Aliment Pharmacol Ther. 2005;21:881\u2013887.","journal-title":"Aliment Pharmacol Ther"},{"key":"5285_CR16","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1097\/00042737-200601000-00013","volume":"18","author":"RC Mallant-Hent","year":"2006","unstructured":"Mallant-Hent RC, Mary B, von Blomberg E, et al. Disappearance of anti-Saccharomyces cerevisiae antibodies in coeliac disease during a gluten-free diet. Eur J Gastroenterol Hepatol. 2006;18:75\u201378.","journal-title":"Eur J Gastroenterol Hepatol"},{"key":"5285_CR17","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1007\/s10875-008-9255-7","volume":"29","author":"S Ashorn","year":"2009","unstructured":"Ashorn S, V\u00e4lineva T, Kaukinen K, et al. Serological responses to microbial antigens in celiac disease patients during a gluten-free diet. J Clin Immunol. 2009;29:190\u2013195.","journal-title":"J Clin Immunol"},{"key":"5285_CR18","doi-asserted-by":"publisher","first-page":"620","DOI":"10.1097\/MCG.0000000000000089","volume":"48","author":"L Viitasalo","year":"2014","unstructured":"Viitasalo L, Niemi L, Ashorn M, et al. Early microbial markers of celiac disease. J Clin Gastroenterol. 2014;48:620\u2013624.","journal-title":"J Clin Gastroenterol"},{"key":"5285_CR19","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1053\/j.gastro.2008.10.013","volume":"136","author":"A Rubio-Tapia","year":"2009","unstructured":"Rubio-Tapia A, Kelly DG, Lahr BD, Dogan A, Wu TT, Murray JA. Clinical staging and survival in refractory celiac disease: a single center experience. Gastroenterology. 2009;136:99\u2013107.","journal-title":"Gastroenterology"},{"key":"5285_CR20","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1136\/gut.2009.195131","volume":"59","author":"A Rubio-Tapia","year":"2010","unstructured":"Rubio-Tapia A, Murray JA. Classification and management of refractory celiac disease. Gut.. 2010;59:547\u2013557.","journal-title":"Gut."},{"key":"5285_CR21","doi-asserted-by":"publisher","first-page":"e76163","DOI":"10.1371\/journal.pone.0076163","volume":"8","author":"J Taavela","year":"2013","unstructured":"Taavela J, Koskinen O, Huhtala H, et al. Validation of morphometric analyses of small-intestinal biopsy readouts in celiac disease. PLoS One. 2013;8:e76163.","journal-title":"PLoS One"},{"key":"5285_CR22","doi-asserted-by":"publisher","first-page":"1332","DOI":"10.1111\/j.1572-0241.2003.07456.x","volume":"98","author":"TT J\u00e4rvinen","year":"2003","unstructured":"J\u00e4rvinen TT, Kaukinen K, Laurila K, et al. Intraepithelial lymphocytes in celiac disease. Am J Gastroenterol. 2003;98:1332\u20131337.","journal-title":"Am J Gastroenterol"},{"key":"5285_CR23","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1053\/gast.2000.8519","volume":"119","author":"CL Sutton","year":"2000","unstructured":"Sutton CL, Kim J, Yamane A, et al. Identification of a novel bacterial sequence associated with Crohn\u2019s disease. Gastroenterology. 2000;119:23\u201331.","journal-title":"Gastroenterology"},{"key":"5285_CR24","doi-asserted-by":"publisher","first-page":"6044","DOI":"10.1128\/IAI.69.10.6044-6054.2001","volume":"69","author":"B Wei","year":"2001","unstructured":"Wei B, Dalwadi H, Gordon LK, et al. Molecular cloning of a Bacteroides caccae TonB-linked outer membrane protein identified by an inflammatory bowel disease marker antibody. Infect Immun. 2001;69:6044\u20136054.","journal-title":"Infect Immun"},{"key":"5285_CR25","doi-asserted-by":"publisher","first-page":"2511","DOI":"10.3748\/wjg.v18.i20.2511","volume":"18","author":"K Kurppa","year":"2012","unstructured":"Kurppa K, R\u00e4s\u00e4nen T, Collin P, et al. Endomysial antibodies predict celiac disease irrespective of the titers or clinical presentation. World J Gastroenterol. 2012;18:2511\u20132516.","journal-title":"World J Gastroenterol"},{"key":"5285_CR26","doi-asserted-by":"publisher","first-page":"516","DOI":"10.1097\/MEG.0b013e32835dca77","volume":"25","author":"S Gross","year":"2013","unstructured":"Gross S, van Wanrooij RL, Tack GJ, et al. Antibody titers against food antigens decrease upon a gluten-free diet, but are not useful for the follow-up of (refractory) celiac disease. Eur J Gastroenterol Hepatol. 2013;25:516\u2013518.","journal-title":"Eur J Gastroenterol Hepatol"},{"key":"5285_CR27","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1097\/00042737-200203000-00017","volume":"14","author":"K Kaukinen","year":"2002","unstructured":"Kaukinen K, Sulkanen S, M\u00e4ki M, Collin P. IgA-class transglutaminase antibodies in evaluating the efficacy of gluten-free diet in coeliac disease. Eur J Gastroenterol Hepatol. 2002;14:311\u2013315.","journal-title":"Eur J Gastroenterol Hepatol"},{"key":"5285_CR28","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1097\/MPG.0b013e318214553a","volume":"53","author":"A Mubarak","year":"2011","unstructured":"Mubarak A, Oudshoorn JH, Kneepkens CM, et al. A child with refractory coeliac disease. J Pediatr Gastroenterol Nutr. 2011;53:216\u2013218.","journal-title":"J Pediatr Gastroenterol Nutr"},{"issue":"7","key":"5285_CR29","doi-asserted-by":"publisher","first-page":"6900","DOI":"10.3390\/nu7085314","volume":"17","author":"MC Cenit","year":"2015","unstructured":"Cenit MC, Olivares M, Codoner-Franch P, Sanz Y. Intestinal microbiota and celiac disease: cause, consequence or co-evolution? Nutrients. 2015;17(7):6900\u20136923.","journal-title":"Nutrients"},{"key":"5285_CR30","doi-asserted-by":"publisher","first-page":"1724","DOI":"10.1016\/j.biochi.2012.03.025","volume":"94","author":"E Nistal","year":"2012","unstructured":"Nistal E, Caminero A, Vivas S, et al. Differences in faecal bacteria populations and faecal bacteria metabolism in healthy adults and celiac disease patients. Biochimie. 2012;94:1724\u20131729.","journal-title":"Biochimie"},{"key":"5285_CR31","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1159\/000442934","volume":"34","author":"G Zhou","year":"2016","unstructured":"Zhou G, Song Y, Yang W, et al. ASCA, ANCA, ALCA and many more: are they useful in the diagnosis of inflammatory bowel disease? Dig Dis. 2016;34:90\u201397.","journal-title":"Dig Dis"},{"key":"5285_CR32","doi-asserted-by":"publisher","first-page":"1105","DOI":"10.1590\/S0100-879X2008001200010","volume":"41","author":"EG Vilela","year":"2008","unstructured":"Vilela EG, Torres HO, Ferrari ML, Lima AS, Cunha AS. Gut permeability to lactulose and mannitol differs in treated Crohn\u2019s disease and celiac disease patients and healthy subjects. Braz J Med Biol Res. 2008;41:1105\u20131109.","journal-title":"Braz J Med Biol Res"},{"key":"5285_CR33","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1097\/00054725-200102000-00002","volume":"7","author":"S Vermeire","year":"2001","unstructured":"Vermeire S, Peeters M, Vlietinck R, et al. Anti-Saccharomyces cerevisiae antibodies (ASCA), phenotypes of IBD, and intestinal permeability: a study in IBD families. Inflamm Bowel Dis. 2001;7:8\u201315.","journal-title":"Inflamm Bowel Dis"},{"key":"5285_CR34","doi-asserted-by":"publisher","first-page":"1281","DOI":"10.1097\/00042737-200312000-00005","volume":"15","author":"M Harrer","year":"2003","unstructured":"Harrer M, Reinisch W, Dejaco C, et al. Do high serum levels of anti-Saccharomyces cerevisiae antibodies result from a leakiness of the gut barrier in Crohn\u2019s disease? Eur J Gastroenterol Hepatol. 2003;15:1281\u20131285.","journal-title":"Eur J Gastroenterol Hepatol"}],"container-title":["Digestive Diseases and Sciences"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s10620-018-5285-z\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s10620-018-5285-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s10620-018-5285-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,9,19]],"date-time":"2019-09-19T19:04:03Z","timestamp":1568919843000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s10620-018-5285-z"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,9,20]]},"references-count":34,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2018,12]]}},"alternative-id":["5285"],"URL":"https:\/\/doi.org\/10.1007\/s10620-018-5285-z","relation":{},"ISSN":["0163-2116","1573-2568"],"issn-type":[{"value":"0163-2116","type":"print"},{"value":"1573-2568","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,9,20]]},"assertion":[{"value":"3 April 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 September 2018","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 September 2018","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"All authors declare that they have no conflict of interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}