From 2-dimensional to 3-dimensional: Overcoming Dilemmas in Intestinal Mucosal Interpretation

Overview

Journal World J Gastroenterol

Publisher Baishideng Publishing Group

Specialty Gastroenterology

Date 2019 Jun 8

PMID 31171885

Citations 1

Authors

Richard Pg Charlesworth

Michael N Marsh

Affiliations

Soon will be listed here.

Abstract

The purpose of this review is to provide a definitive account of small intestinal mucosal structure and interpretation. The coeliac lesion has been well known, but not well described to date and this review aims to identify the interpretative difficulties which have arisen over time with the histological assessment of coeliac disease. In early coeliac interpretation, there were significant inaccuracies, particularly surrounding intraepithelial lymphocyte counts and the degree of villous flattening which occurred in the tissue. Many of these interpretive pitfalls are still encountered today, increasing the potential for diagnostic errors. These difficulties are mostly due to the fact that stained 2-dimensional sections can never truly represent the 3-dimensional framework of the intestinal tissue under investigation. Therefore, this review offers a critical account occasioned by these 2-dimensional interpretative errors and which, in our opinion, should in general be jettisoned. As a result, we leave a framework regarding the true 3-dimensional knowledge of mucosal structure accrued over the 70-year period of study, and one which is available for future reference.

Citing Articles

Diagnosing coeliac disease: Out with the old and in with the new?.

Charlesworth R World J Gastroenterol. 2020; 26(1):1-10.

PMID: 31933510 PMC: 6952296. DOI: 10.3748/wjg.v26.i1.1.

References

Ensari A, Marsh M . Diagnosing celiac disease: A critical overview. Turk J Gastroenterol. 2019; 30(5):389-397. PMC: 6505646. DOI: 10.5152/tjg.2018.18635. View

Creamer B, Leppard P . Post-mortem examination of a small intestine in the coeliac syndrome. Gut. 1965; 6(5):466-71. PMC: 1552328. DOI: 10.1136/gut.6.5.466. View

Watson A, Wright N . Coeliac disease. Morphology and cell kinetics of the jejunal mucosa in untreated patients. Clin Gastroenterol. 1974; 3(1):11-31. View

Quiding-Jarbrink M, Lakew M, Nordstrom I, Banchereau J, Butcher E, Holmgren J . Human circulating specific antibody-forming cells after systemic and mucosal immunizations: differential homing commitments and cell surface differentiation markers. Eur J Immunol. 1995; 25(2):322-7. DOI: 10.1002/eji.1830250203. View

Ensari A, Marsh M . Exploring the villus. Gastroenterol Hepatol Bed Bench. 2018; 11(3):181-190. PMC: 6040026. View

Crowe P, Marsh M . Morphometric analysis of small intestinal mucosa. IV. Determining cell volumes. Virchows Arch A Pathol Anat Histopathol. 1993; 422(6):459-66. DOI: 10.1007/BF01606454. View

Cabanne A, Vazquez H, Argonz J, Moreno M, Nachman F, Niveloni S . Clinical utility of counting intraepithelial lymphocytes in celiac disease intestinal mucosa. Acta Gastroenterol Latinoam. 2007; 37(1):20-8. View

Maki M, Holm K, Koskimies S, Hallstrom O, VISAKORPI J . Normal small bowel biopsy followed by coeliac disease. Arch Dis Child. 1990; 65(10):1137-41. PMC: 1792364. DOI: 10.1136/adc.65.10.1137. View

Sarna V, Skodje G, Reims H, Risnes L, Dahal-Koirala S, Sollid L . HLA-DQ:gluten tetramer test in blood gives better detection of coeliac patients than biopsy after 14-day gluten challenge. Gut. 2017; 67(9):1606-1613. DOI: 10.1136/gutjnl-2017-314461. View

10.

PADYKULA H, STRAUSS E, LADMAN A, GARDNER F . A morphologic and histochemical analysis of the human jejunal epithelium in nontropical sprue. Gastroenterology. 1961; 40:735-65. View

11.

Guix M, Skinner J, Whitehead R . Measuring intraepithelial lymphocytes, surface area, and volume of lamina propria in the jejunal mucosa of coeliac patients. Gut. 1979; 20(4):275-8. PMC: 1412384. DOI: 10.1136/gut.20.4.275. View

12.

Fry L, Seah P, McMinn R, Hoffbrand A . Lymphocytic infiltration of epithelium in diagnosis of gluten-sensitive enteropathy. Br Med J. 1972; 3(5823):371-4. PMC: 1785442. DOI: 10.1136/bmj.3.5823.371. View

13.

Marsh M . Studies of intestinal lymphoid tissue. IV--The predictive value of raised mitotic indices among jejunal epithelial lymphocytes in the diagnosis of gluten-sensitive enteropathy. J Clin Pathol. 1982; 35(5):517-25. PMC: 497709. DOI: 10.1136/jcp.35.5.517. View

14.

Marsh M, Bjarnason I, Shaw J, Ellis A, Baker R, Peters T . Studies of intestinal lymphoid tissue. XIV--HLA status, mucosal morphology, permeability and epithelial lymphocyte populations in first degree relatives of patients with coeliac disease. Gut. 1990; 31(1):32-6. PMC: 1378337. DOI: 10.1136/gut.31.1.32. View

15.

Brottveit M, Beitnes A, Tollefsen S, Bratlie J, Jahnsen F, Johansen F . Mucosal cytokine response after short-term gluten challenge in celiac disease and non-celiac gluten sensitivity. Am J Gastroenterol. 2013; 108(5):842-50. DOI: 10.1038/ajg.2013.91. View

16.

Crowe P, Marsh M . Morphometric analysis of intestinal mucosa. VI--Principles in enumerating intra-epithelial lymphocytes. Virchows Arch. 1994; 424(3):301-6. DOI: 10.1007/BF00194615. View

17.

Toner P, Carr K, Ferguson A, MacKay C . Scanning and transmission electron microscopic studies of human intestinal mucosa. Gut. 1970; 11(6):471-81. PMC: 1553028. DOI: 10.1136/gut.11.6.471. View

18.

Loft D, Marsh M, Crowe P . Rectal gluten challenge and diagnosis of coeliac disease. Lancet. 1990; 336(8720):953. DOI: 10.1016/0140-6736(90)92331-b. View

19.

CRABBE P, Nash D, Bazin H, Eyssen D, Heremans J . Antibodies of the IgA type in intestinal plasma cells of germfree mice after oral or parenteral immunization with ferritin. J Exp Med. 1969; 130(4):723-44. PMC: 2138719. DOI: 10.1084/jem.130.4.723. View

20.

Fottrell P, McNicholl B . Early or pre-coeliac mucosa: development of gluten enteropathy. Gut. 1981; 22(1):65-9. PMC: 1419315. DOI: 10.1136/gut.22.1.65. View