Beyond white light endoscopy: The role of optical biopsy in inflammatory bowel disease

World Journal of Gastroenterology

Volumn 19, Issue 43, 2013, Pages 7544-7551

  Liu, Julia ^a   Dlugosz, Aldona ^b   Neumann, Helmut ^c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Barrier function; Confocal endomicroscopy; Disease relapse; Dysplasia; Endocytoscopy; Mucosal healing; Mucosal inflammation; Optical biopsy

Indexed keywords

INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR;

ARTICLE; BIOPSY; COLONOSCOPY; CONFOCAL LASER MICROSCOPY; CONFOCAL MICROSCOPY; CROHN DISEASE; DYSPLASIA; ENDOCYTOSCOPY; ENTERITIS; FOLLOW UP; HISTOPATHOLOGY; HUMAN; IMAGING; INTESTINE EPITHELIUM; META ANALYSIS (TOPIC); NEOPLASM; PATHOGENESIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); RELAPSE; SENSITIVITY AND SPECIFICITY;

BARRIER FUNCTION; CONFOCAL ENDOMICROSCOPY; DISEASE RELAPSE; DYSPLASIA; ENDOCYTOSCOPY; MUCOSAL HEALING; MUCOSAL INFLAMMATION; OPTICAL BIOPSY;

BIOPSY; ENDOSCOPY, GASTROINTESTINAL; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; INTESTINES; MICROSCOPY, CONFOCAL; OPTICAL IMAGING; PREDICTIVE VALUE OF TESTS; PROGNOSIS; RECURRENCE;

EID: 84888126513     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v19.i43.7544     Document Type: Article

References (58)

1. Neumann H, Kiesslich R, Wallace MB, Neurath MF. Confocal laser endomicroscopy: technical advances and clinical applications. Gastroenterology 2010; 139: 388-392, 392. e1-e2 [PMID: 20561523]
2. Neumann H, Fuchs FS, Vieth M, Atreya R, Siebler J, Kiesslich R, Neurath MF. Review article: in vivo imaging by endocytoscopy. Aliment Pharmacol Ther 2011; 33: 1183-1193 [PMID: 21457290 DOI: 10.1111/j.1365-2036.2011.04647.x]
3. Minami H, Inoue H, Yokoyama A, Ikeda H, Satodate H, Hamatani S, Haji A, Kudo S. Recent advancement of observing living cells in the esophagus using CM double staining: endocytoscopic atypia classification. Dis Esophagus 2012; 25: 235-241 [PMID: 21895852 DOI: 10.1111/ j.1442-2050.2011.01241.x]
4. Neurath MF, Travis SP. Mucosal healing in inflammatory bowel diseases: a systematic review. Gut 2012; 61: 1619-1635 [PMID: 22842618 DOI: 10.1136/gutjnl-2012-302830]
5. Pineton de Chambrun G, Peyrin-Biroulet L, Lémann M, Colombel JF. Clinical implications of mucosal healing for the management of IBD. Nat Rev Gastroenterol Hepatol 2010; 7: 15-29 [PMID: 19949430 DOI: 10.1038/nrgastro.2009.203]
6. Frøslie KF, Jahnsen J, Moum BA, Vatn MH. Mucosal healing in inflammatory bowel disease: results from a Norwegian population-based cohort. Gastroenterology 2007; 133: 412-422 [PMID: 17681162]
7. Baert F, Moortgat L, Van Assche G, Caenepeel P, Vergauwe P, De Vos M, Stokkers P, Hommes D, Rutgeerts P, Vermeire S, D'Haens G. Mucosal healing predicts sustained clinical remission in patients with early-stage Crohn's disease. Gastroenterology 2010; 138: 463-468, quiz e10-e11 [PMID: 19818785 DOI: 10.1053/j.gastro.2009.09.056]
8. Florén CH, Benoni C, Willén R. Histologic and colonoscopic assessment of disease extension in ulcerative colitis. Scand J Gastroenterol 1987; 22: 459-462 [PMID: 3602926]
9. Kiesslich R, Fritsch J, Holtmann M, Koehler HH, Stolte M, Kanzler S, Nafe B, Jung M, Galle PR, Neurath MF. Methylene blue-aided chromoendoscopy for the detection of intraepithelial neoplasia and colon cancer in ulcerative colitis. Gastroenterology 2003; 124: 880-888 [PMID: 12671882 DOI: 10.1053/gast.2003.50146]
10. Neumann H, Vieth M, Atreya R, Neurath MF, Mudter J. Prospective evaluation of the learning curve of confocal laser endomicroscopy in patients with IBD. Histol Histopathol 2011; 26: 867-872 [PMID: 21630216]
11. Watanabe O, Ando T, Maeda O, Hasegawa M, Ishikawa D, Ishiguro K, Ohmiya N, Niwa Y, Goto H. Confocal endomicroscopy in patients with ulcerative colitis. J Gastroenterol Hepatol 2008; 23 Suppl 2: S286-S290 [PMID: 19120913 DOI: 10.1111/j.1440-1746.2008.05559.x]
12. Li CQ, Xie XJ, Yu T, Gu XM, Zuo XL, Zhou CJ, Huang WQ, Chen H, Li YQ. Classification of inflammation activity in ulcerative colitis by confocal laser endomicroscopy. Am J Gastroenterol 2010; 105: 1391-1396 [PMID: 19935787]
13. Neumann H, Vieth M, Atreya R, Grauer M, Siebler J, Bernatik T, Neurath MF, Mudter J. Assessment of Crohn's disease activity by confocal laser endomicroscopy. Inflamm Bowel Dis 2012; 18: 2261-2269 [PMID: 22344873 DOI: 10.1002/ ibd.22907]
14. Schmidt C, Lautenschlaeger C, Collnot EM, Schumann M, Bojarski C, Schulzke JD, Lehr CM, Stallmach A. Nano-and microscaled particles for drug targeting to inflamed intestinal mucosa: a first in vivo study in human patients. J Control Release 2013; 165: 139-145 [PMID: 23127508 DOI: 10.1016/ j.jconrel.2012.10.019]
15. Atreya R, Neumann H, Neufert C, Waldner Mea, Neurath MF. In Vivo Molecular Imaging Using Fluorescent Anti-TNF Antibodies and Confocal LASER Endomicroscopy Predicts Response to Anti-TNF Therapy in Crohn's Disease. Nat Med 2013; In press
16. Bessho R, Kanai T, Hosoe N, Kobayashi T, Takayama T, Inoue N, Mukai M, Ogata H, Hibi T. Correlation between endocytoscopy and conventional histopathology in microstructural features of ulcerative colitis. J Gastroenterol 2011; 46: 1197-1202 [PMID: 21805068 DOI: 10.1007/s00535-011-0439-1]
17. Neumann H, Vieth M, Neurath MF, Atreya R. Endocytoscopy allows accurate in vivo differentiation of mucosal inflammatory cells in IBD: a pilot study. Inflamm Bowel Dis 2013; 19: 356-362 [PMID: 22644957 DOI: 10.1002/ibd.23025]
18. Mescoli C, Albertoni L, D'incá R, Rugge M. Dysplasia in inflammatory bowel diseases. Dig Liver Dis 2013; 45: 186-194 [PMID: 22974564 DOI: 10.1016/j.dld.2012.07.013]
19. Mattar MC, Lough D, Pishvaian MJ, Charabaty A. Current management of inflammatory bowel disease and colorectal cancer. Gastrointest Cancer Res 2011; 4: 53-61 [PMID: 21673876]
20. Itzkowitz SH, Harpaz N. Diagnosis and management of dysplasia in patients with inflammatory bowel diseases. Gastroenterology 2004; 126: 1634-1648 [PMID: 15168373]
21. Vagefi PA, Longo WE. Colorectal cancer in patients with inflammatory bowel disease. Clin Colorectal Cancer 2005; 4: 313-319 [PMID: 15663834]
22. Müller AD, Sonnenberg A. Prevention of colorectal cancer by flexible endoscopy and polypectomy. A case-control study of 32,702 veterans. Ann Intern Med 1995; 123: 904-910 [PMID: 7486484]
23. Collins PD, Mpofu C, Watson AJ, Rhodes JM. Strategies for detecting colon cancer and/or dysplasia in patients with inflammatory bowel disease. Cochrane Database Syst Rev 2006; (2): CD000279 [PMID: 16625534 DOI: 10.1002/14651858. CD000279.pub3]
24. van Rijn JC, Reitsma JB, Stoker J, Bossuyt PM, van Deventer SJ, Dekker E. Polyp miss rate determined by tandem colonoscopy: a systematic review. Am J Gastroenterol 2006; 101: 343-350 [PMID: 16454841 DOI: 10.1111/j.1572-0241.2006.00390.x]
25. Rex DK, Cutler CS, Lemmel GT, Rahmani EY, Clark DW, Helper DJ, Lehman GA, Mark DG. Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies. Gastroenterology 1997; 112: 24-28 [PMID: 8978338]
26. Kaplan GG, Heitman SJ, Hilsden RJ, Urbanski S, Myers RP, Lee SS, Burak KW, Swain M, Panaccione R. Populationbased analysis of practices and costs of surveillance for colonic dysplasia in patients with primary sclerosing cholangitis and colitis. Inflamm Bowel Dis 2007; 13: 1401-1407 [PMID: 17600816 DOI: 10.1002/ibd.20204]
27. Hoffman A, Goetz M, Vieth M, Galle PR, Neurath MF, Kiesslich R. Confocal laser endomicroscopy: technical status and current indications. Endoscopy 2006; 38: 1275-1283 [PMID: 17163333 DOI: 10.1055/s-2006-944813]
28. Goetz M, Toermer T, Vieth M, Dunbar K, Hoffman A, Galle PR, Neurath MF, Delaney P, Kiesslich R. Simultaneous confocal laser endomicroscopy and chromoendoscopy with topical cresyl violet. Gastrointest Endosc 2009; 70: 959-968 [PMID: 19595315 DOI: 10.1016/j.gie.2009.04.016]
29. Kiesslich R, Goetz M, Lammersdorf K, Schneider C, Burg J, Stolte M, Vieth M, Nafe B, Galle PR, Neurath MF. Chromoscopy-guided endomicroscopy increases the diagnostic yield of intraepithelial neoplasia in ulcerative colitis. Gastroenterology 2007; 132: 874-882 [PMID: 17383417 DOI: 10.1053/ j.gastro.2007.01.048]
30. Hurlstone DP, Thomson M, Brown S, Tiffin N, Cross SS, Hunter MD. Confocal endomicroscopy in ulcerative colitis: differentiating dysplasia-associated lesional mass and adenoma-like mass. Clin Gastroenterol Hepatol 2007; 5: 1235-1241 [PMID: 17690019]
31. van den Broek FJ, van Es JA, van Eeden S, Stokkers PC, Ponsioen CY, Reitsma JB, Fockens P, Dekker E. Pilot study of probe-based confocal laser endomicroscopy during colonoscopic surveillance of patients with longstanding ulcerative colitis. Endoscopy 2011; 43: 116-122 [PMID: 21165821 DOI: 10.1055/s-0030-1255954]
32. Su P, Liu Y, Lin S, Xiao K, Chen P, An S, He J, Bai Y. Efficacy of confocal laser endomicroscopy for discriminating colorectal neoplasms from non-neoplasms: a systematic review and meta-analysis. Colorectal Dis 2013; 15: e1-e12 [PMID: 23006609 DOI: 10.1111/codi.12033]
33. Jørgensen KK, Grzyb K, Lundin KE, Clausen OP, Aamodt G, Schrumpf E, Vatn MH, Boberg KM. Inflammatory bowel disease in patients with primary sclerosing cholangitis: clinical characterization in liver transplanted and nontransplanted patients. Inflamm Bowel Dis 2012; 18: 536-545 [PMID: 21456044 DOI: 10.1002/ibd.21699]
34. Lindberg BU, Broomé U, Persson B. Proximal colorectal dysplasia or cancer in ulcerative colitis. The impact of primary sclerosing cholangitis and sulfasalazine: results from a 20-year surveillance study. Dis Colon Rectum 2001; 44: 77-85 [PMID: 11805567]
35. Claessen MM, Lutgens MW, van Buuren HR, Oldenburg B, Stokkers PC, van der Woude CJ, Hommes DW, de Jong DJ, Dijkstra G, van Bodegraven AA, Siersema PD, Vleggaar FP. More right-sided IBD-associated colorectal cancer in patients with primary sclerosing cholangitis. Inflamm Bowel Dis 2009; 15: 1331-1336 [PMID: 19229982 DOI: 10.1002/ibd.20886]
36. Dlugosz A, Barakat AM, Ost A, Bergquist A. Probe-Based Confocal Laser Endomicroscopy in Colonoscopic Surveillance of Patients With PSC-IBD. Gastroenterology 2013; 144 (5(SUP1): S87. Available from: URL: http://www.gastrojournal. org/supplements
37. af Björkesten CG, Nieminen U, Sipponen T, Turunen U, Arkkila P, Färkkilä M. Mucosal healing at 3 months predicts long-term endoscopic remission in anti-TNF-treated luminal Crohn's disease. Scand J Gastroenterol 2013; 48: 543-551 [PMID: 23477356 DOI: 10.3109/00365521.2013.772230]
38. Rutgeerts P, Van Assche G, Sandborn WJ, Wolf DC, Geboes K, Colombel JF, Reinisch W, Kumar A, Lazar A, Camez A, Lomax KG, Pollack PF, D'Haens G. Adalimumab induces and maintains mucosal healing in patients with Crohn' s disease: data from the EXTEND trial. Gastroenterology 2012; 142: 1102-1111. e2 [PMID: 22326435 DOI: 10.1053/ j.gastro.2012.01.035]
39. Colombel JF, Rutgeerts P, Reinisch W, Esser D, Wang Y, Lang Y, Marano CW, Strauss R, Oddens BJ, Feagan BG, Hanauer SB, Lichtenstein GR, Present D, Sands BE, Sandborn WJ. Early mucosal healing with infliximab is associated with improved long-term clinical outcomes in ulcerative colitis. Gastroenterology 2011; 141: 1194-1201 [PMID: 21723220]
40. Kiesslich R, Goetz M, Angus EM, Hu Q, Guan Y, Potten C, Allen T, Neurath MF, Shroyer NF, Montrose MH, Watson AJ. Identification of epithelial gaps in human small and large intestine by confocal endomicroscopy. Gastroenterology 2007; 133: 1769-1778 [PMID: 18054549]
41. Liu JJ, Madsen KL, Boulanger P, Dieleman LA, Meddings J, Fedorak RN. Mind the gaps: confocal endomicroscopy showed increased density of small bowel epithelial gaps in inflammatory bowel disease. J Clin Gastroenterol 2011; 45: 240-245 [PMID: 21030873 DOI: 10.1097/ MCG.0b013e3181fbdb8a]
42. Kiesslich R, Duckworth CA, Moussata D, Gloeckner A, Lim LG, Goetz M, Pritchard DM, Galle PR, Neurath MF, Watson AJ. Local barrier dysfunction identified by confocal laser endomicroscopy predicts relapse in inflammatory bowel disease. Gut 2012; 61: 1146-1153 [PMID: 22115910]
43. Turcotte JF, Wong K, Mah SJ, Dieleman LA, Kao D, Kroeker K, Claggett B, Saltzman JR, Wine E, Fedorak RN, Liu JJ. Increased epithelial gaps in the small intestine are predictive of hospitalization and surgery in patients with inflammatory bowel disease. Clin Transl Gastroenterol 2012; 3: e19 [PMID: 23238291 DOI: 10.1038/ctg.2012.13]
44. Liu JJ, Rudzinski JK, Mah SJ, Thiesen AL, Bao H, Wine E, Ogg SC, Boulanger P, Fedorak RN, Madsen KL. Epithelial gaps in a rodent model of inflammatory bowel disease: a quantitative validation study. Clin Transl Gastroenterol 2011; 2: e3 [PMID: 23237881 DOI: 10.1038/ctg.2011.2]
45. Liu JJ, Wong K, Thiesen AL, Mah SJ, Dieleman LA, Claggett B, Saltzman JR, Fedorak RN. Increased epithelial gaps in the small intestines of patients with inflammatory bowel disease: density matters. Gastrointest Endosc 2011; 73: 1174-1180 [PMID: 21396639]
46. Liu JJ, Rudzinski JK, Mah SJ, Thiesen AL, Bao HY, Wine E, Ogg SC, Boulanger P, Fedorak RN, Madsen KL. Epithelial gaps in a rodent model of inflammatory bowel disease: a quantitative validation study. Clin and Trans Gastro 2011; 2: e3 [PMID: 23237881]
47. Montrose MH. The future of GI and liver research: editorial perspectives: I. Visions of epithelial research. Am J Physiol Gastrointest Liver Physiol 2003; 284: G547-G550 [PMID: 12631555 DOI: 10.1152/ajpgi.00547.2002]
48. Clayburgh DR, Shen L, Turner JR. A porous defense: the leaky epithelial barrier in intestinal disease. Lab Invest 2004; 84: 282-291 [PMID: 14767487]
49. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE. Metagenomic analysis of the human distal gut microbiome. Science 2006; 312: 1355-1359 [PMID: 16741115]
50. Neish AS. Microbes in gastrointestinal health and disease. Gastroenterology 2009; 136: 65-80 [PMID: 19026645]
51. Watson AJ, Duckworth CA, Guan Y, Montrose MH. Mechanisms of epithelial cell shedding in the Mammalian intestine and maintenance of barrier function. Ann N Y Acad Sci 2009; 1165: 135-142 [PMID: 19538298]
52. Ishiguro Y. Mucosal proinflammatory cytokine production correlates with endoscopic activity of ulcerative colitis. J Gastroenterol 1999; 34: 66-74 [PMID: 10204613]
53. Monteleone G, Trapasso F, Parrello T, Biancone L, Stella A, Iuliano R, Luzza F, Fusco A, Pallone F. Bioactive IL-18 expression is up-regulated in Crohn's disease. J Immunol 1999; 163: 143-147 [PMID: 10384110]
54. Moussata D, Goetz M, Gloeckner A, Kerner M, Campbell B, Hoffman A, Biesterfeld S, Flourie B, Saurin JC, Galle PR, Neurath MF, Watson AJ, Kiesslich R. Confocal laser endomicroscopy is a new imaging modality for recognition of intramucosal bacteria in inflammatory bowel disease in vivo. Gut 2011; 60: 26-33 [PMID: 20980342]
55. Neumann H, Günther C, Vieth M, Grauer M, Wittkopf N, Mudter J, Becker C, Schoerner C, Atreya R, Neurath MF. Confocal laser endomicroscopy for in vivo diagnosis of Clostridium difficile associated colitis-a pilot study. PLoS One 2013; 8: e58753 [PMID: 23527018 DOI: 10.1371/journal. pone.0058753]
56. May GR, Sutherland LR, Meddings JB. Is small intestinal permeability really increased in relatives of patients with Crohn's disease? Gastroenterology 1993; 104: 1627-1632 [PMID: 8500719]
57. Meddings JB. Review article: Intestinal permeability in Crohn's disease. Aliment Pharmacol Ther 1997; 11 Suppl 3: 47-53; discussion 53-6 [PMID: 9467978]
58. Liu JJ, Davis EM, Wine E, Lou Y, Rudzinski JK, Alipour M, Boulanger P, Thiesen AL, Sergi C, Fedorak RN, Muruve D, Madsen KL, Irvin RT. Epithelial cell extrusion leads to breaches in the intestinal epithelium. Inflamm Bowel Dis 2013; 19: 912-921 [PMID: 23511029 DOI: 10.1097/ MIB.0b013e3182807600]