Abstract
The present study was undertaken to investigate ultrastructurally the epithelium covering lymphoid nodules obtained from colonoscopic biopsies of the human colon and rectum. Colonoscopy using the dye spraying contrast, method was performed in nine patients who showed x-ray evidence of lymphonodular hyperplasia. Fifty-two colonoscopical biopsy specimens, of lymphoid nodules were obtained from the ascending, transverse, and descending colon and rectosigmoid region. All specimens were observed by light and electron microscopy. Light microscopy disclosed large lymphoid follicles protruding into the lumen with a “dome-type” configuration. These extended to the lamina propria of the mucosa and were associated with a massive lymphoid aggregation extending as far as the muscularis mucosa from the submucosa. The epithelium covering these nodules contained a few goblet cells and many lymphocytes. Observation of the elevated surface at the apex by scanning electron microscopy revealed M cells with sparse microvilli in the dome epithelium surrounded by crypts. Transmission electron microscopy disclosed M cells enfolding many immature or mature lymphocytes and plasmocytes. The M cells had cytoplasmic microvilli (so-called “microfolds”) on their surfaces, well-developed tubulovesicular systems, and vacuoles in the cytoplasm. The basic structure of the M cells as observed by scanning and transmission electron microscopy was the same as that of M cells in the Peyer's patches of humans and mice. The apical surface of the colonic lymphoid follicles in Crohn's disease patients was associated with erosions observed by scanning electron microscopy. The erosions proved to be the naked surface of the dome after removal of the epithelium and many holes from 2.0 to 6.0 μm in diameter were observed on the naked surface. At high magnification, lymphocytes were seen projecting from holes (18%) on the naked surface of the dome. These ultrastructural findings indicate that human colonic lymphoid follicles are very similar to those seen in other species.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Owen RL, Jones AL: Epithelial cell specialization within human Peyer's patches: An ultrastructural study of intestinal lymphoid follicles. Gastroenterology 66:189–203, 1974
Owen RL: Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer's patches in neonatal unobstructed mouse intestine. Gastroenterology 72:440–451, 1977
Wolf JL, Rubin DH, Finberg R, Kauffman RS, Sharpe AH, Trier JS, Fields BN: Intestinal M cells: A pathway for entry of reovirus into the host. Science 212:471–472, 1981
Siciński P, Rowiński J, Warchol JB, Jarzabek S Gut W, Szczygie B, Bielecki, Koch G. Poliovirus type 1 enters the human host through intestinal M cells. Gastroenterology 98:56–58, 1990
Inman LR, Cantey JR: Specific adherence ofEscherichia coli (strain RDEC-1) to membranous (M) cells of the Peyer's patch inEscherichia coli diarrhea in the rabbit. J Clin Invest 71:1–8, 1983
Fujimura Y: Functional morphology of microfold cells (M cells) in Peyer's patches: Phagocytosis and transport of BCG by M cells into rabbit Peyer's patches. Gastroenterol Jpn 21:325–335, 1986
Kohbata S, Yokoyama H, Yabuuchi E: Cytopathogenic effect ofSalmonella typhi GIFU 10007 on M cells of murine ileal Peyer's patches in ligated ileal loop: An ultrastructural study. Microbiol Immunol 30:1225–1237, 1986
Owen RL, Pierce NF, Apple RT Cray WC Jr: M cell transport ofVibrio cholerae from the intestinal lumen into Peyer's patches. A mechanism for antigen sampling and for microbial transepithelial migration. J Infect Dis 153:1108–1118, 1986
Fujimura Y, Ohtani K, Kamoi R, Kato T, Kozuka K, Miyashima N, Uchida J, Kihara T, Mine H: An ultrastructural study of ileal invasion process ofYersinia, pseudotuberculosis in rabbits. J Clin Electron Microsc 22:712–713, 1989
Walker RI, Schmauder-Chock, Paker JL: Selective association and transport ofCampylobacter jejuni through M cells of rabbit Peyer's patches. Can J Microbiol 34:1142–1147, 1988
Wassef JS, Keren DF, Mailloux JL: Role of M cells in intestinal antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect Immun 57:858–863, 1989
Grutzkau A, Hanski C, Hahn H, Riecken EO: Involvement of M cells in the bacterial invasion of Peyer's patches: A common mechanism shared byYersinia enterocolitica and other enteroinvasive bacteria Gut 31:1011–1015, 1990
Fujimura Y, Arita S, Kihara T: Uptake of BCG into immunized and nonimmunized rabbit Peyer's patches-morphology and quantitative analysis. Kawasaki Med J 16:181–190, 1990
O'Leary AD, Sweeney EC: Lymphoglandular complexes of the colon: Structure and distribution. Histopathology 10: 267–283, 1986
Jacob E, Backer SJ, Swaminathan SP: “M” cells in the follicle-associated epithelium of the human colon. Histopathology 11:941–952, 1987
Owen RL, Nemanic P: Antigen processing structures of the mammalian intestinal tract: An SEM study of lymphoepithelial organs. Scanning Electron Microsc Part II:367–378, 1978
Uchida J: Electron microscopic study of microfold cells (M cells) in normal and inflamed human appendix. Gastroenterol Jpn 23:251–262, 1988
Hoshi H, Mori T: Identification of the bursa-dependent and thymus-dependent areas in tonsilla caecalis of chickens. Tohoku J Exp Med 111:309–322, 1973
Atkins AM, Schofield GC: Lymphoglandular complexes in the large intestine of the dog. J Anat 113:169–178, 1972
Bland PW, Britton D: Morphological study of antigensampling structures in the rat large intestine. Infect Immun 43:693–699, 1984
Owen RL, Bass DM, Piazza AJ: Colonic lymphoid patches: A portal of entry in mice for type 1 reovirus administered anally. Gastroenterology 89:A468, 1990 (abstract)
Kealy WF: Colonic lymphoid-glandular complex (microbursa): Nature and morphology. J Clin Pathol 29:241–244, 1976
Tada M, Katoh S, Kohli Y, Kawai K: On the dye spraying method in colonofiberscopy. Endoscopy 8:70–74, 1976
Kelvin FM, Oddson TA, Rice RP, Garbutt JT, Bradenham BP: Double contrast barium enema in Crohn's disease and ulcerative colitis. Am J Roentgenol 131:207–213, 1978
Ell SR, Frank PH: Spectrum of lymphoid hyperplasia: Colonic manifestations sarcoidosis, infectious mononucleosis and Crohn's disease. Gastrointest Radiol 6:329–332, 1981
Kaplan B, Benson J, Rothstein F, Dahms B, Halpin T: Lymphonodular hyperplasia of the colon as a pathologic finding in children with lower gastrointestinal bleeding. J Pediatr Gastroenterol Nutr 3:704–708, 1984
Venkitachalam PS, Hirsch E, Elguezabal A, Littman L: Multiple lymphoid polyposis and familial polyposis of the colon: A genetic relationship. Dis Colon Rectum 21:336–341, 1978
De smet AA, Turbergen DG, Martel W: Nodular lymphoid hyperplasia of the colon associated with dysgammaglobulinemia. Am J Roentgenol 127:515–517, 1976
Crooks DJM, Brown WR: The distribution of intestinal nodular lymphoid hyperplasia in immunoglobulin deficiency. Clin Radiol 31:701–706, 1980
Brown RA, Glick SN, Teplick SK: Diffuse lymphoid follicles of the colon associated with colonic carcinoma. Am J Roentgenol 142:105–109, 1983
Burbige EJ, Sobky Reda ZF: Endoscopic appearance of colonic lymphoid nodules: A normal variant. Gastroenterology 72:524–526, 1977
Riddlesberger MM, Leventhal E: Nodular colonic mucosa of childhood: Normal or pathologic? Gastroenterology 79:265–270, 1980
Kenney PJ, Koehler RE, Shackelford GD: The clinical significance of large lymphoid follicles of the colon. Radiology 142:41–46, 1982
Laufer I, deSa D: Lymphoid follicular pattern: A normal feature of the pediatric colon.. Am J Roentgenol 130:51–55, 1978
Cornes JS: Number, size, and distribution of Peyer's patches in the human small intestine. Gut 6:225–233, 1965
Dukes C, Bussey HJR: The number of lymphoid follicles of the human large intestine. J Pathol Bacteriol 29:111–116 1926
Kelvin FM, Max RJ, Norton GA, Oddson TA, Rice RP, Thompson WM, Garbutt JT: Lymphoid follicular pattern of the colon in adults. Am J Roentgenol 133:821–825, 1979
Langman JM, Rowland R: The number and distribution of lymphoid follicles in the human large intestine. J Anat 194:189–194, 1986
Ahronheim GA: The transmission of AIDS. Nature 313:534, 1985
Evans BA, Dawson SG, Mclean KA, Teece SA, Key PR, Bond RA, Macrae KD, Jesson WJ, Mortimer PP: Sexual lifestyle and clinical findings related to HTLV-III/LAV status in homosexual men. Genitourin Med 62:384–389, 1986
Smith MW, Peacock MA: “M” cell distribution in follicleassociated epithelium of mouse Peyer's patch. Am J Anat 159:167–175, 1980
Smith MW, Peacock MA: Lymphocyte induced formation of antigen transporting “M” cells from fully differentiated mouse enterocytes.In Mechanisms of Intestinal Adaptation. JWL Robinson, RH Dowling, EO Riecken (eds). Lancaster, MTP Press, 1982, pp 573–583
Bhalla DK, Owen RL: Cell renewal and migration in lymphoid follicles of Peyer's patches, and cecum—an autoradiographic study in mice. Gastroenterology 82:232–242, 1982
Bye WA, Allan CH, Trier JS: Structure, distribution, and origin of M cells in Peyer's patches of mouse ileum. Gastroenterology 86:789–801, 1984
Fujimura Y, Kihara T, Ohtani K, Kamoi R, Kato T, Kozuka K, Miyashima N, Uchida J: Distribution of microfold cells (M cells) in human follicle-associated epithelium. Gastroenterol Jpn 25:130, 1990
Rickert RR, Carter HW: The “early” ulcerative lesion of Crohn's disease: Correlative light- and scanning electronmicroscopic studies. J Clin Gastroenterol 2:11–19, 1980
Crouse DA, Perry GA, Murphy BO, Sharp JG: Characteristics of submucosal lymphoid tissue located in the proximal colon of the rat. J Anat 162:53–65, 1989
Owen RL, Piazza AJ, Ermak TH: Ultrastructural and cytoarchitectural features of lymphoreticular organs in the colon and rectum of adult BALB/c mice. Am J Anat 190:10–18, 1991
Shimazui T: An ultrastructural study of the pathway and the location of migrating lymphocytes through the intestinal microfold cells (M cells). J Clin Electron Microsc 18:127–140, 1985
McClugage SG, Low FN, Zimny ML: Porsity, of the basement membrane overlying Peyer's patches in rats and monkeys. Gastroenterology 91:1128–1133, 1986
Cerf-Bensussan N, Quaroni A, Kurnick JT, Bhan AK: Intraepithelial lymphocytes modulate Ia expression by intestinal epithelial cells. J Immunol 132:2244–2251, 1984
Scott H, Solheim BG, Brandtzaeg P, Thorsby E: HLA-DR antigens in the epithelium of the human small intestine. Scand J Immunol 12:77–82, 1980
Natali PG, De Martino G, Quaranta V, Nicotra RM, Frezza F, Pellegrino MA, Ferrone S: Expression of Ia-like antigens in normal human nonlymphoid tissue. Transplantation 31:75–78, 1981
Hirata I, Austin LL, Blackwell WH, Weber JR, Dobbins WO III: Immunoelectron microscopic localization of HLA-DR antigen in control small intestine and colon and in inflammatory, bowel disease. Dig Dis Sci 31:1317–1330, 1986
Lynch HT, Frozen P, Schuelke GS: Hereditary colon cancer; polyposis and nonpolyposis variants. CA 35:95–114, 1985
Bland PW, Britton DC: Colonic lymphoid tissue and its influence on tumor induction in dimethylhydrazine-treated rats. Br J Cancer 4:275, 1981
Nauss KM, Locniskar M, Pavlina T, Newberne PM: Morphology and distribution of 1,2-dimethylhydrazine dihydrochloride-induced colon tumors and their relationship to gut-associated lymphoid tissue in the rat. J Natl Cancer Inst 73:915–924, 1984
Oohara T, Ogino A, Tohma H: Microscopic adenomas in non-polyposis coli: Incidence and relation to basal cells and lymphoid follicles. Dis Colon Rectum 24:120–126, 1981
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Fujimura, Y., Hosobe, M. & Kihara, T. Ultrastructural study of M cells from colonic lymphoid nodules obtained by colonoscopic biopsy. Digest Dis Sci 37, 1089–1098 (1992). https://doi.org/10.1007/BF01300292
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01300292