Skip to main content
PMC home page
Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 2004 Feb 5;65(1):59–63. doi: 10.1016/S0034-5288(98)90028-5

Evaluation of B and T lymphocytes and plasma cells in colonic mucosa from healthy dogs and from dogs with inflammatory bowel disease

J Stonehewer 1, JW Simpson 1, RW Else 2, N MacIntyre 2
PMCID: PMC7172459  PMID: 9769074

Abstract

The aim of this study was to investigate the subpopulations of lymphocytes in the colonic mucosa of healthy dogs and dogs with inflammatory bowel disease (IBD). Fourteen normal dogs and 13 dogs with IBD were examined. Endoscopic biopsy specimens of colonic mucosa from each dog were stained specifically for pan T lymphocytes (CD3) and pan B lymphocytes (CD79a), and for plasma cells with methyl green pyronin (MGP) stain. Cells were counted by means of a grid and statistical analysis was performed on the data collected. B and T lymphocytes were also counted in the glandular epithelium of normal dogs and dogs with IBD and the normal and abnormal groups compared statistically. Healthy dogs had significantly lower numbers of T cells in the lamina propria and glandular epithelium and significantly lower numbers of B cells in the lamina propria. Significant group differences for plasma cells were not evident. Our results indicate that in IBD a chronic cellular immune reaction is present in the diseased gut involving increased numbers of B and T lymphocytes.

References

  1. Anderson N.V. 2nd edn. Lea and Febiger; Pennsylvania, USA: 1992. Veterinary Gastroenterology. [Google Scholar]
  2. Bienenstock J. The mucosal immunological network. Annals of Allergy. 1984;53:535–540. [PubMed] [Google Scholar]
  3. Berk J.E. 4th edn. Vol. 4. W.B. Saunders Company; Philadelphia, USA: 1985. pp. 2108–2118. (Bockus Gastroenterology). [Google Scholar]
  4. Blakemore J.C. Gastrointestinal allergy. Veterinary Clinics of North America: Small Animal Practice. 1994;24(4):655–695. doi: 10.1016/s0195-5616(94)50077-9. [DOI] [PubMed] [Google Scholar]
  5. Brandtzaeg P., Halstensen T.S., Kett K. Immunobiology and immunopathology of human gut mucosa: Humoral immunity and intraepithelial lymphocytes. Gastroenterology. 1989;97:1562–1584. doi: 10.1016/0016-5085(89)90406-x. [DOI] [PubMed] [Google Scholar]
  6. Burrows C.F. Canine Colitis. The Compendium of Continuing Education October. 1992:1347–1354. [Google Scholar]
  7. Carman P.S., Ernst P.B., Rosenthal K.L. Intrapithelial leukocytes contain a unique subpopulation of NK-like cytotoxic cells active in the defense of gut epithelium of enteric murine coronaviruses. Journal of Immunology. 1986;136:1548–1553. [PubMed] [Google Scholar]
  8. Cerf-Bensussan N., Schneeberger E.E., Bhan A.K. Immunohistologic and immunoelectron microscopic characterisation of the mucosal lymphocytes of human small intestine by the use of monoclonal antibodies. Journal of Immunology. 1983;130:2615–2622. [PubMed] [Google Scholar]
  9. Clancy R. Isolation and kinetic characteristics of mucosal lymphocytes in Crohn's disease. Gastroenterology. 1976;70:177–180. [PubMed] [Google Scholar]
  10. Deusch K., Reich K. Immunological aspects of inflammatory bowel disease. Endoscopy. 1992;24:568–577. doi: 10.1055/s-2007-1010547. [DOI] [PubMed] [Google Scholar]
  11. Eade O.E., St Andre-Ukena S., Moulton C., Macpherson B., Beeken W.L. Lymphocyte subpopulations of intestinal mucosa in inflammatory bowel disease. Gut. 1980;21:675–682. doi: 10.1136/gut.21.8.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fell J.M.E., Walker-Smith J.A., Spencer J., MacDonald T.T. The distribution of dividing T cells throughout the intestinal wall in inflammatory bowel disease (IBD) Clinical Experienced Immunology. 1996;104:280–285. doi: 10.1046/j.1365-2249.1996.999701.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Green F.H.Y., Fox H. The distribution of mucosal antibodies in the bowel of patients with Crohn's disease. Gut. 1975;16:125–131. doi: 10.1136/gut.16.2.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Guilford W.G., Center S.A., Strombeck D.R., Williams D.A., Meyer D.J. 3rd edn. W.B. Saunders; Philadelphia, USA: 1996. Strombeck's Small Animal Gastroenterology. [Google Scholar]
  15. Halliwell R.E.W. The sites of production and localisation of IgE in canine tissues. Annals N.Y. Academy Sciences. 1975;254:476–488. doi: 10.1111/j.1749-6632.1975.tb29195.x. [DOI] [PubMed] [Google Scholar]
  16. Hart I.R. The distribution of immunoglobulin-containing cells in canine small intestine. Research in Veterinary Science. 1979;27:269–274. [PubMed] [Google Scholar]
  17. Harty R.F., Leibach J.R. Immune disorders of the gastrointestinal tract and liver. Medicine Clinics of North America. 1985;69:675–703. doi: 10.1016/s0025-7125(16)31014-8. [DOI] [PubMed] [Google Scholar]
  18. Hirata L., Berrebi G., Austin L.L., Keren D.F., Dobbins W.O., III Immunohistochemical characterisation of intraepithelial and lamina propria lymphocytes in control ileum and colon and in inflammatory bowl disease. Digestive Diseases and Sciences. 1986;31(6):593–603. doi: 10.1007/BF01318690. [DOI] [PubMed] [Google Scholar]
  19. Hoang P., Senju M., Lowes J.R., Jewell D.P. Phenotypic characterisation of isolated intraepithelial lymphocytes in patients and ulcerative colitis and normal controls. Digestive Diseases and Sciences. 1992;37(11):1725–1728. doi: 10.1007/BF01299866. [DOI] [PubMed] [Google Scholar]
  20. Hsu Su-Ming, Raine L. Protein A, avidin and biotin in immunohistochemistry. J. Histochem. Cytochem. 1981;29:1349–1353. doi: 10.1177/29.11.6172466. [DOI] [PubMed] [Google Scholar]
  21. Jenkins D., Goodall A., Drew K., Scott B.B. What is colitis? Statistical approach to distinguishing clinically important inflammatory change in rectal biopsy specimens. Journal of Clinical Pathology. 1988;41:72–79. doi: 10.1136/jcp.41.1.72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jergens A.E., Moore F.M., Haynes J.S., Miles K.G. Idiopathic inflammatory bowel disease in dogs and cats: 84 cases (1987–1990) JAVMA. 1992;201(10):1603–1608. [PubMed] [Google Scholar]
  23. Jergens A.E., Moore F.M., Kaiser M.S., Haynes J.S., Kinyon J.M. Morphometric evaluation of immunoglobulin A-containing and immunoglobulin G-containing cells and T cells in duodenal mucosa from healthy dogs and from dogs with inflammatory bowel disease or nonspecific gastroenteritis. AJVR. 1996;57(5):697–704. [PubMed] [Google Scholar]
  24. Keren D.F., Appelman H.D., Dobbins W.O., III, Wells J.J., Whisenant B., Foley J., Dieterle R., Geisinger K. Correlation of histopathologic evidence of disease activity with the immunoglobulin containing cells in the colon of patients with inflammatory bowel disease. Human Pathology. 1984;15:757–763. doi: 10.1016/s0046-8177(84)80167-7. [DOI] [PubMed] [Google Scholar]
  25. Kirsner J.B., Shorter R.G. Recent developments in nonspecific inflammatory bowel disease. New England Journal of Medicine. 1982;306(14):837–848. doi: 10.1056/NEJM198204083061404. [DOI] [PubMed] [Google Scholar]
  26. Korelitz B.I., Sohn N. Grune and Stratton, Inc; Orlando, Florida, USA: 1985. Inflammatory bowel disease: Experience and controversy; pp. 43–50. [Google Scholar]
  27. Leib M.S., Hiler L.A., Roth L., Thatcher C., Monroe W.E., Shell L.G. Plasmacytic lymphocytic colitis in the dog. Seminars in Veterinary Medicine and Surgery (small animal) 1989;4(3):241–246. [PubMed] [Google Scholar]
  28. Magne M.L. Vol. 7. 1992. Pathophysiology of inflammatory bowel disease; pp. 112–116. (Seminars in Veterinary Medicine and Surgery (small animal)). (2) [PubMed] [Google Scholar]
  29. Markowitz J., Daum F. Summary of the proceedings of the subcommittee on immunosuppressive use in IBD. Vol. 12. 1991. Immunology of inflammatory bowel disease; pp. 411–423. (Journal of Pediatric Gastroenterology and Nutrition). [PubMed] [Google Scholar]
  30. Meuwissen S.G.M., Feltkamp-Vroom Thea M., Brutel De La Rivière A., Von Dem Borne A.E.G.K.R., Tytgat G.N. Analysis of the lympho-plasmacytic infiltrate in Crohn's disease with special reference to identification of lymphocyte-subpopulations. Gut. 1976;17:770–780. doi: 10.1136/gut.17.10.770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Read R.A. Treatment of canine nictitans plasmacytic conjunctivitis with 0·2 per cent cyclosporin ointment. JSAP. 1995;36:50–56. doi: 10.1111/j.1748-5827.1995.tb02821.x. [DOI] [PubMed] [Google Scholar]
  32. Roitt I., Brostoff J., Male D. 4th edn. Times Mirror International Publishers Ltd; London: 1996. Immunology; pp. 2.1–2.18. [Google Scholar]
  33. Roth L., Walton A.M., Leib M.S., Burrows C.F. A grading system for lymphocytic plasmacytic colitis in dogs. Journal of Veterinary Diagnosis and Investigation. 1990;2:257–262. doi: 10.1177/104063879000200401. [DOI] [PubMed] [Google Scholar]
  34. Sacher D.B., Auslander M.O., Walfish J.S. Aetiological theories of inflammatory bowel disease. Clinics of Gastroenterology. 1980;9(2):231–257. [PubMed] [Google Scholar]
  35. Selby W.S., Janossy G., Jewell D.P. Immunohistological characterisation of intraepithelial lymphocytes of human gastrointestinal tract. Gut. 1981;22:169–176. doi: 10.1136/gut.22.3.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Selby W.S., Janossy G., Bofill M., Jewell D.P. Intestinal lymphocyte subpopulations in inflammatory bowel disease: An analysis by immumohistological and cell isolation techniques. Gut. 1984;25:32–40. doi: 10.1136/gut.25.1.32. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Seldenrijk C.A., Morson B.C., Meuwissen S.G.M., Schipper N.W., Lindeman J., Meijer C.J.L.M. Histopathological evaluation of colonic mucosal biopsy specimens in chronic inflammatory bowel disease: diagnostic implications. Gut. 1991;32:1514–1520. doi: 10.1136/gut.32.12.1514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Shanahan F. Pathogenesis of ulcerative colitis. The Lancet. 1993;342:407–411. doi: 10.1016/0140-6736(93)92818-e. [DOI] [PubMed] [Google Scholar]
  39. Shanahan F. Current concepts of the pathogenesis of inflammatory bowel disease. International Journal of Medical Science. 1993;163(12):544–549. doi: 10.1007/BF02943022. [DOI] [PubMed] [Google Scholar]
  40. Shorter R.G., Kirsner J.B. Grune and Stratton Inc; Orlando, Florida, USA: 1985. Gastrointestinal immunity for the clinician; pp. 171–187. [Google Scholar]
  41. Shorter R.G., Shephard D.A.E. Frontiers in inflammatory bowel disease. Digestive Diseases. 1975;20(6):540–571. doi: 10.1007/BF01071174. [DOI] [PubMed] [Google Scholar]
  42. Shorter R.G., Tomasi T.B., Huizenga K.A., Spencer R.J., Stobo J.D. The immunology of chronic ulcerative colitis and Crohn's disease. Annals of New York Academy of Science. 1976;278:586–591. doi: 10.1111/j.1749-6632.1976.tb47073.x. [DOI] [PubMed] [Google Scholar]
  43. Strickland R.G., Husby G., Black W.C., Williams R.C., Jr eripheral blood and intestinal lymphocyte sub-populations in Crohn's disease. Gut. 1975;16:847–853. doi: 10.1136/gut.16.11.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Strober W. Animal models of inflammatory bowel disease - an overview. Digestive Diseases and Sciences. 1985;30(12):3S–10S. doi: 10.1007/BF01296964. [DOI] [PubMed] [Google Scholar]
  45. Strober W., James S.P. The immunological basis of inflammatory bowel disease. Journal of Clinical Immunology. 1986;6(6):415–432. doi: 10.1007/BF00915248. [DOI] [PubMed] [Google Scholar]
  46. Thompson E.M., Price A.B., Altman D.G., Shoter C., Slavin G. Quantitation in inflammatory bowel disease using computerised interactive image analysis. Journal of Clinical Pathology. 1985;38:631–638. doi: 10.1136/jcp.38.6.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Vaerman J.P., Heremans J.F. Distribution of various immunoglobulin containing cells in canine lymphoid tissue. Immunology. 1969;17:627–633. [PMC free article] [PubMed] [Google Scholar]
  48. Van Der Heijden P.J., Stok W. Improved procedure for the isolation of functionally active lymphoid cells from the murine intestine. Journal of Immunological Methods. 1987;103:161–167. doi: 10.1016/0022-1759(87)90285-7. [DOI] [PubMed] [Google Scholar]
  49. Van Garderen E., Van Dijk J.E., Van Den Ingh T.S. Intestinal intraepithelial lymphocyte: A review of the literature. Veterinary Questions. 1991;13:225–232. doi: 10.1080/01652176.1991.9694312. [DOI] [PubMed] [Google Scholar]
  50. Willard M.D., Williams J.F., Stowe H.D. Number and distribution of IgM cells and IgA cells in colonic tissue of conditioned sex- and breed-matched dogs. American Journal of Veterinary Research. 1982;43:688–692. [PubMed] [Google Scholar]
  51. Zeroogian J.M., Chopra S. Collagenous colitis and lymphocytic colitis. Annual Review of Medicine. 1994;45:105–118. doi: 10.1146/annurev.med.45.1.105. [DOI] [PubMed] [Google Scholar]

Articles from Research in Veterinary Science are provided here courtesy of Elsevier

RESOURCES