J. clin. Path., 1976, 29, 241-244

Colonic lymphoid-glandular complex (microbursa):nature and morphologyW. F. KEALY

From the Departments of Morbid Anatomy, King's College Hospital, London and Kingston Hospital,Kingston-on-Thames, Surrey

SYNOPSIS A study of lymphoid-glandular complexes of the large bowel has been undertaken.Sections from 1924 surgical colectomy and proctocolectomy specimens were examined, andlymphoid-glandular complexes were observed in 231. It has been shown that they are distributedthroughout the large bowel and occur in all age groups and in normal and disease states. Ananalogy has been drawn between them, the palatine tonsils, and the bursa of Fabricius. It is con-

cluded that the lymphoid-glandular complex is, most probably, a normal structural entity of thelarge bowel and that it acts as a local receptor of antigenic material for future immune recognition.It is suggested that microbursa rather than lymphoid-glandular complex is a more apt name forthis structure.

The lymphoid tissue of the colon is distributed aslymphoid nodules or aggregates in close appositionto the muscularis mucosae, either below it in theupper part of the submucosa, above it in the laminapropria, lying between its muscle fibres or fillinggaps in its substance. The overlying mucosa may beseen, at times, to protrude through these gaps in themuscularis mucosae to a variable extent in closeassociation with the underlying lymphoid nodulewith which it forms an intimate lymphoid-glandular(L-G) complex (fig 1). Clark (1969, 1970) describedsimilar structures, referring to them as micro-diverticula, and he discussed their importance inrelation to granulomatous ileocolitis and ulcerativecolitis. Dyson (1975) referred to them as glandularhemiations and described a possible mode of theirdevelopment in ulcerative colitis.A study of L-G complexes of the large bowel has

been undertaken in an effort to determine the natureof these structures.

Methods

Standard blocks for section, about 4 cm in length,were taken from the ascending, transverse, descen-ding, and sigmoid regions of necropsy specimens ofcolon but autolysis hindered detailed examination,a point stressed by Lumb (1960), and this method wasabandoned.

Received for publication 4 September 1975241

Alternatively, sections from surgical partial andtotal colectomy and proctocolectomy specimens atKing's College Hospital and Kingston Hospitalwere studied, covering the years 1965-74 and 1958-74respectively, and examined for the presence of L-Gcomplexes. The site of excision, age, sex, and patho-logical diagnosis of each specimen were noted fromsurgical reports, day books, and, when necessary,from case notes.

Results

Altogether sections from 1924 specimens wereexamined. One or more L-G complexes were foundin sections from 231 specimens. Of these, 33 werepresent in specimens of caecum and ascending colon,nine in specimens of transverse colon, and 172 inspecimens of descending colon and rectum. L-Gcomplexes were present in 17 total colectomyspecimens but the sites from which the blocks weretaken were not ascertainable. The distribution ofL-G complexes and the number of each type ofspecimen examined are shown in the table. Of the 17total colectomy specimens showing L-G complexes,15 were from cases of ulcerative colitis, one ofCrohn's disease, and one of diverticular disease. Thedisease processes in which L-G complexes occurredare as follows: primary carcinoma, carcinoma withdiverticular disease, diverticular disease, ulcerativecolitis, Crohn's disease, non-specific inflammation,polyps, intussusception, volvulus, Hirschsprung's

W. F Kealy

Fig 1 Colon showingtwoL-G complexes(HandE x 30).

.,

Caecum Transverse Descending Totaland Colon Colon and ColectomyAscending RectumColon

No. ofspecimens 383 73 1397 71No. of L-G complexes 33 9 172 17Percentage incidence 8-6 12-3 12-3 23-9

Table Number ofspecimens examinedand those showingL-G complexes

disease, and vascular lesions. They were found alsoin two specimens which showed no gross or micro-scopic abnormality, one from a 1-year-old girl withimperforate anus, from whom a short length ofdescending colon was removed, and the other froma 34-year-old man from whom the caecum and partof the ascending colon were excised.The youngest specimen in which L-G complexes

were present was from the female child mentionedpreviously; the oldest was from a woman of 86 withcarcinoma of the rectum. L-G complexes werepresent in specimens from all age groups between1 year and 86 years, though sections from 12specimens in the age group 91-100 did not reveal any.

SITES OF L-G COMPLEXESSerial sections through several separate surgicalblocks of colon, both parallel and perpendicular tothe mucosa, showed that the gaps in the muscularis

mucosae are true defects filled with lymphoid tissue,and lymphocytes could be seen between the fibresof the adjacent muscularis mucosae (fig 2). Lympho-cytes were also seen inside the epithelial cytoplasmof some L-G complexes.Measurement of the ratios of the maximum

transverse diameters of the lymphoid nodules to thewidths of the gaps in the muscularis mucosaeshowed that increased size of the lymphoid noduleswas paralleled by an increase in width of the gap.No correlation was demonstrated between the extentof protrusion of the mucosa through the gaps withthe diameters of the lymphoid nodules and the widthsof the gaps in the muscularis mucosae.

Discussion

The results show that L-G complexes occur through-out the whole length of the large bowel, that theyoccur in normal and disease states, and that they arepresent in all age groups. Dyson makes the pointthat these structures are herniations of mucosalepithelium through gaps in the muscularis mucosaeand that the initiating factor in their formation islikely to be sustained contraction of the muscularismucosae, thus suggesting that they are acquired.The increase in number of L-G complexes in

sections of ulcerative colitis and Crohn's disease maybe more apparent than real, as in these conditionsthe protrusion of mucosa through gaps in the

242

C..WE":-.r"

Colonic lymphoid-glandular complex (microbursa): nature and morphology

Fig 2 Section taken inthe sameplane as thesurface ofthe mucosashowing a lymphoidnodule inside a gap inthe muscularis mucosae(H and E x 30).

muscularis mucosae may not represent true L-Gcomplexes, as they are often unassociated withlymphoid nodules and are possibly foci of re-epithel-ialization following destruction of the muscularismucosae in these inflammatory states. Histologicalexamination of L-G complexes often showeddegenerative changes in some of the constituentglands. In no case, however, was cellular atypicalitysufficient to warrant a diagnosis of carcinoma. But,in one case of carcinoma, malignant epitheliumcould be seen streaming through a nearby gap in themuscularis mucosae into the underlying lymphoidnodule, which may partly explain the occurrence ofearly metastases from some small carcinomas of thecolon.

Cases of colitis cystica profunda, a rare disease ofthe colon associated with the presence of epithelial-lined mucus-filled cysts in the submucosa, weredescribed by Goodall and Sinclair (1957), whothought that the cysts developed from epitheliumwhich had extended into the submucosa during thehealing of small deep follicular ulcers followingnecrosis of the submucosal lymphoid nodules.Wayte and Helwig (1967) considered that the cystsresulted from extension of surface mucosa alonggranulation tissue tracts created through themuscularis mucosae. Epstein et al (1966) thoughtthat they may develop from herniation of mucosathrough a muscularis mucosae congenitally weak or

damaged by inflammation or perhaps by re-epithel-ialization of deep undermining ulcers. The latterauthors noted that the cysts were never observed inassociation with lymphoid nodules. It would seemtherefore that L-G complexes, which occur com-monly, which are present in all age groups, in allparts of the large bowel, are entities distinct from thecysts of colitis cystica profunda.What then is the nature of these L-G complexes?

It seems likely that they are normal structures of thebowel and are the immunological watchdogs whichcan be easily reached by antigenic material presentin the bowel lumen and which can gain easy accessto the lymphoid tissue through the gaps in themuscularis mucosae and across the single layer ofepithelium that separates it from the underlyinglymphoid nodule. Structures morphologically similarto L-G complexes are present in the small bowel. Ananalogy may be drawn between L-G complexes andthe crypts of the palatine tonsils which are lined bystratified squamous epithelium and dip into thelymphoid tissue, rendering the tonsils more effectiveimmunologically. The bursa of Fabricius, a round orpear-shaped lymphoid diverticulum in the hindgutof birds, lined by pseudostratified epithelium, bearssome morphological resemblance to the L-G com-plex when viewed in this context. It is suspected thatmammals have an equivalent tissue, perhaps morewidely distributed and forming the lymphoid tissue

243

244

of the appendix, the colon, and Peyer's patches ofthe small intestine (Walter and Israel, 1974). Micro-bursae rather than L-G complexes may be a moreapt name for these structures.

I wish to thank Dr M. E. A. Powell, KingstonHospital, for criticism and advice; Professor E. A.Wright, King's College Hospital and Dr J. H. Earle,Queen Mary's Hospital, Roehampton, for access tosurgical sections; Mr J. Spicer, Kingston Hospital,fortechnical assistance; and Miss B. R. Hume fortyping this paper. The work was supported by a grantfrom the South West Thames Regional HealthAuthority for the purchase of photomicrographicequipment.

This paper constitutes part of the work for anMD thesis to be submitted to the National Univer-sity of Ireland.

W. F. Kealy

ReferencesClark, R. M. (1969). Microdiverticula: a possible cause of

granulomatous ileocolitis. Canad. med. Ass. J., 100,1025-1031.

Clark, R. M. (1970). Microdiverticula and submucosalepithelial elements in ulcerative and granulomatousdiseases of the ileum and colon. Canad. med. Ass. J., 103,24-28.

Dyson, J. L. (1975). Herniation of mucosal epithelium intothe submucosa in chronic ulcerative colitis. J. clin. Path.,28, 189-194.

Epstein, S. E., Ascari, W. Q., Ablow, R. C., Seaman, W. B.,and Lattes, R. (1966). Colitis cystica profunda. Amer. J.clin. Path., 45, 186-201.

Goodall, H. B., and Sinclair, f. S. R. (1957). Colitis cysticaprofunda. J. Path. Bact., 73, 33-42.

Lumb, G. (1960). Normal human rectal mucosa and itsmechanism of repair. Amer. J. dig. Dis., 5, 836-840.

Walter, J. B. and Israel, M. S. (1974). General Pathology, 4thedition, p. 149. Churchill Livingstone, Edinburgh.

Wayte, D. M., and Helwig, E. B. (1967). Colitis cysticaprofunda. Amer. J. clin. Path., 48, 159-169.