An update on diagnostic and prognostic biomarkers in inflammatory bowel disease

References

• Day AS, Ledder O, Leach ST, et al. Crohns and colitis in children and adolescents. World J Gastroenterol. 2012;18:5862–5869.
   PubMed Web of Science ®Google Scholar
• IBD Working Group of the European Society for Paediatric Gastroenterology, Hepatology and Nutrition. Inflammatory bowel disease in children and adolescents: recommendations for diagnosis – the Porto criteria. J Pediatr Gastroenterol Nutr. 2005;41:1–7.
   PubMed Web of Science ®Google Scholar
• Van Limbergen J, Russell RK, Drummond HE, et al. Definition of phenotypic characteristics of childhood onset inflammatory bowel disease. Gastroenterology. 2008;135:1114–1122.
   PubMed Web of Science ®Google Scholar
• Benchimol EI, Fortinsky KJ, Gozdyra P, et al. Epidemiology of pediatric inflammatory bowel disease: a systematic review of international trends. Inflamm Bowel Dis. 2011;17:423–439.
   PubMed Web of Science ®Google Scholar
• Gearry RB, Richardson A, Frampton CM, et al. High incidence of Crohn’s disease in Canterbury, New Zealand: results of an epidemiologic study. Inflamm Bowel Dis. 2006;12:936–943.
   PubMed Web of Science ®Google Scholar
• Su H, Gupta V, As D, et al. Rising incidence of inflammatory bowel disease in Canterbury, New Zealand. Inflamm Bowel Dis. 2016;22:2238–2244.
   PubMed Web of Science ®Google Scholar
• Ng WK, Wong SH, Ng SC. Changing epidemiological trends of inflammatory bowel disease in Asia. Intest Res. 2016 Apr;14(2):111–119.
   PubMed Web of Science ®Google Scholar
• Shah SC, Colombel JF, Sands BE, et al. Systematic review with meta-analysis: mucosal healing is associated with improved long-term outcomes in Crohn’s disease. Aliment Pharmacol Ther. 2016;43:317–333.
   PubMed Web of Science ®Google Scholar
• Sidler MA, Leach ST, Day AS. Fecal S100A12 and fecal calprotectin as noninvasive markers for inflammatory bowel disease in children. Inflamm Bowel Dis. 2008;14:359–366.
   PubMed Web of Science ®Google Scholar
• Mack DR, Langton C, Markowitz J, et al. Laboratory values for children with newly diagnosed inflammatory bowel disease. Pediatrics. 2007;119:1113–1119.
   PubMed Web of Science ®Google Scholar
• Day AS, Hamilton D, Leach ST, et al. Inflammatory markers in children with newly diagnosed inflammatory bowel disease. J Gastroenterol Hepatol Res. 2016;5:2132–2135.
   Google Scholar
• Roseth AG, Fagerhol MK, Aadland E, et al. Assessment of the neutrophil dominating protein calprotectin in feces. A methodologic study. Scand J Gastroenterol. 1992;27:793–798.
   PubMed Web of Science ®Google Scholar
• Tibble J, Teahon K, Thjodleifsson B, et al. A simple method for assessing intestinal inflammation in Crohn’s disease. Gut. 2000;47:506–513.
   PubMed Web of Science ®Google Scholar
• Konikoff MR, Denson LA. Role of fecal calprotectin as a biomarker of intestinal inflammation in inflammatory bowel disease. Inflamm. Bowel Dis. 2006;12:524–534.
   PubMed Web of Science ®Google Scholar
• St L, As D. S100 proteins in the pathogenesis and diagnosis of inflammatory bowel disease. Expert Rev Clin Immunol. 2006;2:471–480.
   PubMedGoogle Scholar
• Sohnle PG, Collins-Lech C, Wiessner JH. The zinc-reversible antimicrobial activity of neutrophil lysates and abscess fluid supernatants. J Infect Dis. 1991;164:137–142.
   PubMed Web of Science ®Google Scholar
• Sohnle PG, Hunter MJ, Hahn B, et al. Zinc-reversible antimicrobial activity of recombinant calprotectin (migration inhibitory factor-related proteins 8 and 14). J Infect Dis. 2000;182:1272–1275.
   PubMed Web of Science ®Google Scholar
• Roseth AG, Schmidt PN, Fagerhol MK. Correlation between faecal excretion of indium-111-labelled granulocytes and calprotectin, a granulocyte marker protein, in patients with inflammatory bowel disease. Scand J Gastroenterol. 1999;34:50–54.
   PubMed Web of Science ®Google Scholar
• Fagerhol MK, Dale I, Andersson T. A radioimmunoassay for a granulocyte protein as a marker in studies on the turnover of such cells. Bull Eur Physiopathol Respir. 1980;16(Suppl):273–282.
   PubMedGoogle Scholar
• Lugering N, Stoll R, Kucharzik T, et al. Immunohistochemical distribution and serum levels of the Ca(2+)-binding proteins MRP8, MRP14 and their heterodimeric form MRP8/14 in Crohn’s disease. Digestion. 1995;56:406–414.
   PubMed Web of Science ®Google Scholar
• Mork G, Schjerven H, Mangschau L, et al. Proinflammatory cytokines upregulate expression of calprotectin (L1 protein, MRP-8/MRP-14) in cultured human keratinocytes. Br J Dermatol. 2003;149:484–491.
   PubMed Web of Science ®Google Scholar
• Brandtzaeg P, Dale I, Fagerhol MK. Distribution of a formalin-resistant myelomonocytic antigen (L1) in human tissues. I. Comparison with other leukocyte markers by paired immunofluorescence and immunoenzyme staining. Am J Clin Pathol. 1987;87:681–699.
   PubMed Web of Science ®Google Scholar
• Du L, Foshaug R, Huang VW, et al. Within-stool and within-day sample variability of fecal calprotectin in patients with inflammatory bowel disease: a prospective observational study. J Clin Gastroenterol. 2016;8:647–650.
   Google Scholar
• Meling TR, Aabakken L, Roseth A, et al. Faecal calprotectin shedding after short-term treatment with non-steroidal anti-inflammatory drugs. Scand J Gastroenterol. 1996;31:339–344.
   PubMed Web of Science ®Google Scholar
• Berni Canani R, Rapacciuolo L, Romano MT, et al. Diagnostic value of faecal calprotectin in paediatric gastroenterology clinical practice. Dig Liver Dis. 2004;36:467–470.
   PubMedGoogle Scholar
• Rugtveit J, Fagerhol MK. Age-dependent variations in fecal calprotectin concentrations in children. J Pediatr Gastroenterol Nutr. 2002;34:323–324.
   PubMed Web of Science ®Google Scholar
• Cerrillo E, Beltrán B, Pous S, et al. Fecal calprotectin in ileal Crohn’s disease: relationship with magnetic resonance enterography and a pathology score. Inflamm Bowel Dis. 2015;21:1572–1579.
   PubMed Web of Science ®Google Scholar
• Miranda LP, Tao T, Jones A, et al. Total chemical synthesis and chemotactic activity of human S100A12 (EN-RAGE). FEBS Lett. 2001;488:85–90.
   PubMed Web of Science ®Google Scholar
• Yang Z, Tao T, Raftery MJ, et al. Proinflammatory properties of the human S100 protein S100A12. J Leukoc Biol. 2001;69:986–994.
   PubMed Web of Science ®Google Scholar
• de Jong NS, Leach ST, Day AS. Fecal S100A12: a novel noninvasive marker in children with Crohn’s disease. Inflamm Bowel Dis. 2006;12:566–572.
   PubMed Web of Science ®Google Scholar
• Day AS, Ehn M, Gearry RB, et al. Fecal S100A12 in healthy infants and children. Dis Markers. 2013;35:295–299.
   PubMed Web of Science ®Google Scholar
• Kaiser T, Langhorst J, Wittkowski H, et al. Faecal S100A12 as a non-invasive marker distinguishing inflammatory bowel disease from irritable bowel syndrome. Gut. 2007;56:1706–1713.
   PubMed Web of Science ®Google Scholar
• Foell D, Kane D, Bresnihan B, et al. Expression of the pro-inflammatory protein S100A12 (EN-RAGE) in rheumatoid and psoriatic arthritis. Rheumatology. 2003;42:1383–1389.
   PubMed Web of Science ®Google Scholar
• Foell D, Seeliger S, Vogl T, et al. Expression of S100A12 (EN-RAGE) in cystic fibrosis. Thorax. 2003;58:613–617.
   PubMed Web of Science ®Google Scholar
• Martins CA, Fonteles MG, Barrett LJ, et al. Correlation of lactoferrin with neutrophilic inflammation in body fluids. Clin Diagn Lab Immunol. 1995;2:763–765.
   PubMedGoogle Scholar
• Langhorst J, Elsenbruch S, Koelzer J, et al. Noninvasive markers in the assessment of intestinal inflammation in inflammatory bowel diseases: performance of fecal lactoferrin, calprotectin, and PMN-elastase, CRP, and clinical indices. Am J Gastroenterol. 2008;103:162–169.
   PubMed Web of Science ®Google Scholar
• Caccaro R, D’Inca R, Martinato M, et al. Fecal lactoferrin and intestinal permeability are effective non-invasive markers in the diagnostic work-up of chronic diarrhea. Biometals. 2014;27:1069–1076.
   PubMed Web of Science ®Google Scholar
• Sugi K, Saitoh O, Hirata I, et al. Fecal lactoferrin as a marker for disease activity in inflammatory bowel disease: comparison with other neutrophil-derived proteins. Am J Gastroenterol. 1996;91:927–934.
   PubMed Web of Science ®Google Scholar
• Silberer H, Kuppers B, Mickisch O, et al. Fecal leukocyte proteins in inflammatory bowel disease and irritable bowel syndrome. Clin Lab. 2005;51:117–126.
   PubMed Web of Science ®Google Scholar
• Wang Y, Pei F, Wang X, et al. Diagnostic accuracy of fecal lactoferrin for inflammatory bowel disease: a meta-analysis. Int J Clin Exp Pathol. 2015;8:12319–12332.
   PubMed Web of Science ®Google Scholar
• Judd TA, Day AS, Lemberg DA, et al. Update of fecal markers of inflammation in inflammatory bowel disease. J Gastroenterol Hepatol. 2011;26:1493–1499.
   PubMed Web of Science ®Google Scholar
• Walker TR, Land ML, Kartashov A, et al. Fecal lactoferrin is a sensitive and specific marker of disease activity in children and young adults with inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2007;44:414–422.
   PubMed Web of Science ®Google Scholar
• Mazurek S. Pyruvate kinase type M2: a key regulator of the metabolic budget system in tumor cells. Int J Biochem Cell Biol. 2011;43:969–980.
   PubMed Web of Science ®Google Scholar
• Sipos F, Molnar B, Zagoni T, et al. Growth in epithelial cell proliferation and apoptosis correlates specifically to the inflammation activity of inflammatory bowel diseases: ulcerative colitis shows specific p53- and EGFR expression alterations. Dis Colon Rectum. 2005;48:775–786.
   PubMed Web of Science ®Google Scholar
• Chung-Faye G, Hayee B, Maestranzi S, et al. Fecal M2-pyruvate kinase (M2-PK): a novel marker of intestinal inflammation. Inflamm Bowel Dis. 2007;13:1374–1378.
   PubMed Web of Science ®Google Scholar
• As D, Judd T, Da L, et al. Fecal M2-PK in children with Crohn’s disease: a preliminary report. Dig Dis Sci. 2012;57(8):2166–2170.
   PubMed Web of Science ®Google Scholar
• Nahidi L, Leach ST, Sidler MA, et al. Osteoprotegerin in pediatric Crohn’s disease and the effects of exclusive enteral nutrition. Inflamm Bowel Dis. 2011;17:516–523.
   PubMed Web of Science ®Google Scholar
• Saiki T. Myeloperoxidase concentrations in the stool as a new parameter of inflammatory bowel disease. Kurume Med J. 1998;45:69–73.
   PubMedGoogle Scholar
• Vitali R, Stronati L, Negroni A, et al. Fecal HMGB1 is a novel marker of intestinal mucosal inflammation in pediatric inflammatory bowel disease. Am J Gastroenterol. 2011;106:2029–2040.
   PubMed Web of Science ®Google Scholar
• Annahazi A, Molnar T, Farkas K, et al. Fecal MMP-9: a new noninvasive differential diagnostic and activity marker in ulcerative colitis. Inflamm Bowel Dis. 2013;19:316–320.
   PubMed Web of Science ®Google Scholar
• Kapel N, Benahmed N, Morali A, et al. Fecal beta-defensin-2 in children with inflammatory bowel diseases. J Pediatr Gastroenterol Nutr. 2009;48:117–120.
   PubMed Web of Science ®Google Scholar
• Aomatsu T, Imaeda H, Matsumoto K, et al. Faecal chitinase 3-like-1: a novel biomarker of disease activity in paediatric inflammatory bowel disease. Aliment Pharmacol Ther. 2011;34:941–948.
   PubMed Web of Science ®Google Scholar
• Koukos G, Polytarchou C, Kaplan JL, et al. MicroRNA-124 regulates STAT3 expression and is down-regulated in colon tissues of pediatric patients with ulcerative colitis. Gastroenterology. 2013;145:842–52.e2.
   PubMed Web of Science ®Google Scholar
• Rech J, Hueber AJ, Finzel S, et al. Prediction of disease relapses by multibiomarker disease activity and autoantibody status in patients with rheumatoid arthritis on tapering DMARD treatment. Ann Rheum Dis. 2016;75:1637–1644.
   PubMed Web of Science ®Google Scholar
• Ganepola GA, Rutledge JR, Suman P, et al. Novel blood-based microRNA biomarker panel for early diagnosis of pancreatic cancer. World J Gastrointest Oncol. 2014;6:22–33.
   PubMedGoogle Scholar
• Kalla R, Kennedy NA, Ventham NT, et al. Serum calprotectin: a novel diagnostic and prognostic marker in inflammatory bowel diseases. Am J Gastroenterol. 2016;111:1796–1805.
   PubMed Web of Science ®Google Scholar
• Leach ST, Yang Z, Messina I, et al. Serum and mucosal S100 proteins, calprotectin (S100A8/S100A9) and S100A12, are elevated at diagnosis in children with inflammatory bowel disease. Scand J Gastroenterol. 2007;42:1321–1331.
   PubMed Web of Science ®Google Scholar
• Boschetti G, Garnero P, Moussata D, et al. Accuracies of serum and fecal S100 proteins (calprotectin and calgranulin C) to predict the response to TNF antagonists in patients with Crohn’s disease. Inflamm Bowel Dis. 2015;21:331–336.
   PubMed Web of Science ®Google Scholar
• Baugh MD, Evans GS, Hollander AP, et al. Expression of matrix metalloproteases in inflammatory bowel disease. Ann NY Acad Sci. 1998;859:249–253.
   PubMed Web of Science ®Google Scholar
• Medina C, Radomski MW. Role of matrix metalloproteinases in intestinal inflammation. J Pharmacol Exp Ther. 2006;318:933–938.
   PubMed Web of Science ®Google Scholar
• Kofla-Dlubacz A, Matusiewicz M, Krzystek-Korpacka M, et al. Correlation of MMP-3 and MMP-9 with Crohn’s disease activity in children. Dig Dis Sci. 2012;57:706–712.
   PubMed Web of Science ®Google Scholar
• Kofla-Dlubacz A, Matusiewicz M, Krzesiek E, et al. Metalloproteinase-3 and −9 as novel markers in the evaluation of ulcerative colitis activity in children. Adv Clin Exp Med. 2014;23:103–110.
   PubMed Web of Science ®Google Scholar
• Bonneau J, Dumestre-Perard C, Rinaudo-Gaujous M, et al. Systematic review: new serological markers (anti-glycan, anti-GP2, anti-GM-CSF Ab) in the prediction of IBD patient outcomes. Autoimmunity Rev. 2015;14:231–245.
   PubMed Web of Science ®Google Scholar
• Tibble JA, Sigthorsson G, Bridger S, et al. Surrogate markers of intestinal inflammation are predictive of relapse in patients with inflammatory bowel disease. Gastroenterology. 2000;119:15–22.
   PubMed Web of Science ®Google Scholar
• Kovacs M, Muller KE, Papp M, et al. New serological markers in pediatric patients with inflammatory bowel disease. World J Gastroenterol. 2014;20:4873–4882.
   PubMed Web of Science ®Google Scholar
• Dubinsky MC. Serologic and laboratory markers in prediction of the disease course in inflammatory bowel disease. World J Gastroenterol. 2010;16:2604–2608.
   PubMed Web of Science ®Google Scholar
• Costa F, Mumolo MG, Ceccarelli L, et al. Calprotectin is a stronger predictive marker of relapse in ulcerative colitis than in Crohn’s disease. Gut. 2005;54:364–368.
   PubMed Web of Science ®Google Scholar
• Guardiola J, Lobaton T, Rodriguez-Alonso L, et al. Fecal levels of calprotectin identifies histologic inflammation in patients with ulcerative colitis in clinical and endoscopic remission. Clin Gastroenterol Hepatol. 2014;12:1865–1870.
   PubMed Web of Science ®Google Scholar
• Walkiewicz D, Werlin SL, Fish D, et al. Fecal calprotectin is useful in predicting disease relapse in pediatric inflammatory bowel disease. Inflamm Bowel Dis. 2008;14:669–673.
   PubMed Web of Science ®Google Scholar
• Mooiweer E, Severs M, Schipper ME, et al. Low fecal calprotectin predicts sustained clinical remission in inflammatory bowel disease patients: a plea for deep remission. J Crohns Colitis. 2015;9:50–55.
   PubMed Web of Science ®Google Scholar
• Bortlik M, Duricova D, Machkova N, et al. Discontinuation of anti-tumor necrosis factor therapy in inflammatory bowel disease patients: a prospective observation. Scand J Gastroenterol. 2016;51:196–202.
   PubMed Web of Science ®Google Scholar
• Diamanti A, Colistro F, Basso MS, et al. Clinical role of calprotectin assay in determining histological relapses in children affected by inflammatory bowel diseases. Inflamm Bowel Dis. 2008;14:1229–1235.
   PubMed Web of Science ®Google Scholar
• Mao R, Yl X, Gao X, et al. Fecal calprotectin in predicting relapse of inflammatory bowel diseases: a meta-analysis of prospective studies. Inflamm Bowel Dis. 2012;18:1894–1899.
   PubMed Web of Science ®Google Scholar
• Dabtriz J, Langhorst J, Lugering A, et al. Improving relapse prediction in inflammatory bowel disease by neutrophil-derived S100A12. Inflamm Bowel Dis. 2013;19:1130–1138.
   PubMed Web of Science ®Google Scholar
• De Cruz P, Kamm MA, Hamilton AL, et al. Crohn’s disease management after intestinal resection: a randomised trial. Lancet. 2015;385:1406–1417.
   PubMed Web of Science ®Google Scholar
• Wright EK, Kamm MA, De Cruz P, et al. Measurement of fecal calprotectin improves monitoring and detection of recurrence of Crohn’s disease after surgery. Gastroenterology. 2015;148:938–947.
   PubMed Web of Science ®Google Scholar
• Orlando A, Modesto I, Castiglione F, et al. The role of calprotectin in predicting endoscopic post-surgical recurrence in asymptomatic Crohn’s disease: a comparison with ultrasound. Eur Rev Med Pharmacol Sci. 2006;10:17–22.
   PubMedGoogle Scholar
• Boschetti G, Laidet M, Moussata D, et al. Levels of fecal calprotectin are associated with the severity of postoperative endoscopic recurrence in asymptomatic patients with Crohn’s disease. Am J Gastroenterol. 2015;110:865–872.
   PubMed Web of Science ®Google Scholar
• Herranz Bachiller MT, Barrio Andres J, Fernandez Salazar L, et al. The utility of faecal calprotectin to predict post-operative recurrence in Crohńs disease. Scand J Gastroenterol. 2016;51:720–726.
   PubMed Web of Science ®Google Scholar
• Desir B, Amre DK, Lu S-E, et al. Utility of serum antibodies in determining clinical course in pediatric Crohn’s disease. Clin Gasterenterol Hepatol. 2004;2:139–146.
   PubMed Web of Science ®Google Scholar
• Plevy S, Silverberg MS, Lockton S, et al. Combined serological, genetic and inflammatory markers differentiate non-IBD, Crohn’s disease and ulcerative colitis patients. Inflamm Bowel Dis. 2013;19:1139–1148.
   PubMed Web of Science ®Google Scholar
• Siegel CA, Horton H, Siegel LS, et al. A validated web-based tool to display individualised Crohn’s disease predicted outcomes based on clinical, serologic and genetic variables. Aliment Pharmacol Ther. 2016;43:262–271.
   PubMed Web of Science ®Google Scholar
• Waterman M, Knight J, Dinani A, et al. Predictors of outcome in ulcerative Colitis. Inflamm Bowel Dis. 2015;21:2097–2105.
   PubMed Web of Science ®Google Scholar
• Paul S, Boschetti G, Rinaudo-Gaujous M, et al. Association of anti-glycan antibodies and inflammatory bowel disease course. J Crohns Colitis. 2015;9:445–451.
   PubMed Web of Science ®Google Scholar
• Sładek M, Wasilewska A, Swiat A, et al. Serum anti-glycan antibodies in paediatric-onset Crohn’s disease: association with disease phenotype and diagnostic accuracy. Prz Gastroenterol. 2014;9:232–241.
   PubMedGoogle Scholar
• Hamilton AL, Kamm MA, De Cruz P, et al. Serologic antibodies in relation to outcome in post-operative Crohn’s disease. J Gastroenterol Hepatol. 2017;11:191-203.
   Google Scholar
• Choung RS, Princen F, Stockfisch TP, et al. Serologic microbial associated markers can predict Crohn’s disease behaviour years before disease diagnosis. Aliment Pharmacol Ther. 2016;43:1300–1310.
   PubMed Web of Science ®Google Scholar
• Van Schaik FD, Oldenburg B, Hart AR, et al. Serological markers predict inflammatory bowel disease years before the diagnosis. Gut. 2013;62:683–688.
   PubMed Web of Science ®Google Scholar