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. 1973 Jun;26(6):427–434. doi: 10.1136/jcp.26.6.427

Staining procedures for the endocrine cells of the upper gastrointestinal mucosa: Light-electron microscopic correlation for the gastrin-producing cell

Sergio A Bencosme 1,2, Juan Lechago 1,2
PMCID: PMC477775  PMID: 4124158

Abstract

Although histochemical, immunohistochemical, and electron microscopic methods have led to the identification of a large variety of endocrine cells in the upper gastrointestinal mucosa, no conventional light microscopic technique capable of the simultaneous identification of these cells has been reported. Such a staining method would be of considerable value to the pathologist as the malfunction of the endocrine cells of the gut, which produce numerous digestive hormones and biogenic amines, is closely related to a number of clinical conditions afflicting man. In this work, after testing three different polychrome staining methods, it has been concluded that a slightly modified Herlant's tetrachrome in tissues fixed in Zenker-formol is the procedure of choice. This method allows the distinction of several different cell types in the upper gastrointestinal mucosa of man and dog and permits the easy identification of the gastrin-producing cells on a routine basis. This identification has been confirmed in the case of two patients with gastrin cell hyperplasia, seen by both light and electron microscopy. Herlant's tetrachrome has proven valuable in the screening of human as well as experimental gastrointestinal tissues and it has been found to be very suitable for recognizing gastrin-producing cell hyperplasias. The usefulness of this method is expected to increase with the establishment of further correlations between the light and electron microscopy of the endocrine cells of the gut.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aures D., Håkanson R., Owman C. Formation and storage of amines in endocrine cells of gastric mucosa. J Neurovisc Relat. 1970;31(4):337–349. doi: 10.1007/BF02312736. [DOI] [PubMed] [Google Scholar]
  2. BENCOSME S. A. Studies on the methods of staining the islet cells of the pancreas. AMA Arch Pathol. 1952 Jan;53(1):87–97. [PubMed] [Google Scholar]
  3. Black W. C., 3rd Enterochromaffin cell types and corresponding carcinoid tumors. Lab Invest. 1968 Nov;19(5):473–486. [PubMed] [Google Scholar]
  4. Black W. C., Haffner H. E. Diffuse hyperplasia of gastric argyrophil cells and multiple carcinoid tumors. An historical and ultrastructural study. Cancer. 1968 Jun;21(6):1080–1099. doi: 10.1002/1097-0142(196806)21:6<1080::aid-cncr2820210609>3.0.co;2-1. [DOI] [PubMed] [Google Scholar]
  5. Bussolati G., Capella C., Solcia E., Vassallo G., Vezzadini P. Ultrastructural and immunofluorescent investigations on the secretin cell in the dog intestinal mucosa. Histochemie. 1971;26(3):218–227. doi: 10.1007/BF00305655. [DOI] [PubMed] [Google Scholar]
  6. Bussolati G., Pearse A. G. Immunofluorescent localization of the gastrin-secreting G cells in the pyloric antrum of the pig. Histochemie. 1970;21(1):1–4. doi: 10.1007/BF00304798. [DOI] [PubMed] [Google Scholar]
  7. Byrnes D. J., Young J. D., Chisholm D. J., Lazarus L. Serum gastrin in patients with peptic ulceration. Br Med J. 1970 Jun 13;2(5710):626–629. doi: 10.1136/bmj.2.5710.626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. CAMPBELL A. C., GOWENLOCK A. H., PLATT D. S., SNOW P. J. A beta-hydroxytryptophan-secreting carcinoid tumour. Gut. 1963 Mar;4:61–67. doi: 10.1136/gut.4.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Capella C., Solcia E., Vassallo G. Identification of six types of endocrine cells in the gastrointestinal mucosa of the rabbit. Arch Histol Jpn. 1969 Aug;30(5):479–495. doi: 10.1679/aohc1950.30.479. [DOI] [PubMed] [Google Scholar]
  10. Creutzfeldt W., Arnold R., Creutzfeldt C., Feurle G., Ketterer H. Gastrin and G-cells in the antral mucosa of patients with pernicious anaemia, acromegaly and hyperparathyroidism and in a Zollinger-Ellison tumour of the pancreas. Eur J Clin Invest. 1971 Sep;1(6):461–479. doi: 10.1111/j.1365-2362.1971.tb00558.x. [DOI] [PubMed] [Google Scholar]
  11. Emås S., Borg I., Fyrö B. Antral and duodenal gastrin activity in non-ulcer and ulcer patients. Scand J Gastroenterol. 1971;6(1):39–43. doi: 10.3109/00365527109180667. [DOI] [PubMed] [Google Scholar]
  12. FREISEN S. R., TRACY H. J., GREGORY R. A. Mechanism of the gastric hypersecretion in the Zollinger-Ellison syndrome: successful extraction of gastrin-like activity from metastases and primary pancreatico-duodenal islet cell carcinoma. Ann Surg. 1962 Feb;155:167–174. doi: 10.1097/00000658-196200000-00001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. FYROE B. ANTRAL GASTRIN ACTIVITY IN DUODENAL AND GASTRIC ULCERS. Gastroenterology. 1964 Jan;46:1–7. [PubMed] [Google Scholar]
  14. Forssmann W. G., Orci L., Pictet R., Renold A. E., Rouiller C. The endocrine cells in the epithelium of the gastrointestinal mucosa of the rat. An electron microscope study. J Cell Biol. 1969 Mar;40(3):692–715. doi: 10.1083/jcb.40.3.692. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Forssmann W. G., Orci L. Ultrastructure and secretory cycle of the gastrin-producing cell. Z Zellforsch Mikrosk Anat. 1969;101(3):419–432. doi: 10.1007/BF00335578. [DOI] [PubMed] [Google Scholar]
  16. Friesen S. R., Bolinger R. E., Pearse A. G., McGuigan J. E. Serum gastrin levels in malignant Zollinger-Ellison Syndrome after total gastrectomy and hypophysectomy. Ann Surg. 1970 Sep;172(3):504–521. doi: 10.1097/00000658-197009000-00014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. GREGORY R. A., TRACY H. J., FRENCH J. M., SIRCUS W. Extraction of a gastrin-like substance from a pancreatic tumour in a case of Zollinger-Ellison syndrome. Lancet. 1960 May 14;1(7133):1045–1048. doi: 10.1016/s0140-6736(60)90932-6. [DOI] [PubMed] [Google Scholar]
  18. Greider M. H., Steinberg V., McGuigan J. E. Electron microscopic identification of the gastrin cell of the human antral mucosa by means of immunocytochemistry. Gastroenterology. 1972 Oct;63(4):572–583. [PubMed] [Google Scholar]
  19. Grossman M. I. Gastrointestinal hormones. Med Clin North Am. 1968 Nov;52(6):1297–1303. [PubMed] [Google Scholar]
  20. HELLERSTROEM C., HELLMAN B. Some aspects of silver impregnation of the islets of Langerhans in the rat. Acta Endocrinol (Copenh) 1960 Dec;35:518–532. doi: 10.1530/acta.0.xxxv0518. [DOI] [PubMed] [Google Scholar]
  21. Håkanson R., Owman C., Sporrong B., Sundler F. Electron microscopic classification of amine-producing endocrine cells by selective staining of ultra-thin sections. Histochemie. 1971;27(3):226–242. doi: 10.1007/BF00264395. [DOI] [PubMed] [Google Scholar]
  22. Kraicer J., Herlant M., Duclos P. Changes in adenohypophyseal cytology and nucleic acid content in the rat 32 days after bilateral adrenalectomy and the chronic injection of cortisol. Can J Physiol Pharmacol. 1967 Nov;45(6):947–956. doi: 10.1139/y67-112. [DOI] [PubMed] [Google Scholar]
  23. Lechago J., Bencosme S. A. The endocrine elements of the digestive system. Int Rev Exp Pathol. 1973;12:119–201. [PubMed] [Google Scholar]
  24. McGuigan J. E., Greider M. H. Correlative immuncchemical and light microscopic studies of the gastrin cell of the antral mucosa. Gastroenterology. 1971 Feb;60(2):223–236. [PubMed] [Google Scholar]
  25. McGuigan J. E., Trudeau W. L. Immunochemical measurement of elevated levels of gastrin in the serum of patients with pancreatic tumors of the Zollinger-Ellison variety. N Engl J Med. 1968 Jun 13;278(24):1308–1313. doi: 10.1056/NEJM196806132782402. [DOI] [PubMed] [Google Scholar]
  26. OBERHELMAN H. A., Jr, NELSEN T. S., JOHNSON A. N., Jr, DRAGSTEDT L. R., 2nd Ulcerogenic tumors of the duodenum. Ann Surg. 1961 Feb;153:214–227. doi: 10.1097/00000658-196115320-00008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Pearse A. G., Bussolati G. Immunofluorescence studies on the distribution of gastrin cells in different clinical states. Gut. 1970 Aug;11(8):646–648. doi: 10.1136/gut.11.8.646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pearse A. G., Bussolati G. The identification of gastrin cells as G cells. Virchows Arch A Pathol Pathol Anat. 1972;355(2):99–104. doi: 10.1007/BF00556312. [DOI] [PubMed] [Google Scholar]
  29. Pearse A. G. Common cytochemical and ultrastructural characteristics of cells producing polypeptide hormones (the APUD series) and their relevance to thyroid and ultimobranchial C cells and calcitonin. Proc R Soc Lond B Biol Sci. 1968 May 14;170(1018):71–80. doi: 10.1098/rspb.1968.0025. [DOI] [PubMed] [Google Scholar]
  30. Pearse A. G., Coulling I., Weavers B., Friesen S. The endocrine polypeptide cells of the human stomach, duodenum, and jejunum. Gut. 1970 Aug;11(8):649–658. doi: 10.1136/gut.11.8.649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Polak J. M., Bloom S., Coulling I., Pearse A. G. Immunofluorescent localization of enteroglucagon cells in the gastrointestinal tract of the dog. Gut. 1971 Apr;12(4):311–318. doi: 10.1136/gut.12.4.311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Polak J. M., Bloom S., Coulling I., Pearse A. G. Immunofluorescent localization of secretin in the canine duodenum. Gut. 1971 Aug;12(8):605–610. doi: 10.1136/gut.12.8.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Polak J. M., Doe W., Coulling I., Pearse A. G. The G cells in pernicious anaemia. Gut. 1971 Apr;12(4):319–323. doi: 10.1136/gut.12.4.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rbin W. Proliferation of endocrine-like enterochromaffin) cells in atrophic gastri mucosa. Gastroenterology. 1969 Dec;57(6):641–648. [PubMed] [Google Scholar]
  35. SANDLER M., SNOW P. J. An atypical carcinoid tumour secreting 5-hydroxytryptophan. Lancet. 1958 Jan 18;1(7012):137–139. doi: 10.1016/s0140-6736(58)90616-0. [DOI] [PubMed] [Google Scholar]
  36. STEMPAK J. G., WARD R. T. AN IMPROVED STAINING METHOD FOR ELECTRON MICROSCOPY. J Cell Biol. 1964 Sep;22:697–701. doi: 10.1083/jcb.22.3.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sasagawa T., Kobayashi S., Fujita T. The endocrine cells in the human pyloric antrum. An electron microscope study of biopsy materials. Arch Histol Jpn. 1970 Sep;32(3):275–288. doi: 10.1679/aohc1950.32.275. [DOI] [PubMed] [Google Scholar]
  38. Soga J., Tazawa K. Pathologic analysis of carcinoids. Histologic reevaluation of 62 cases. Cancer. 1971 Oct;28(4):990–998. doi: 10.1002/1097-0142(1971)28:4<990::aid-cncr2820280424>3.0.co;2-k. [DOI] [PubMed] [Google Scholar]
  39. Thompson J. C., Hirose F. M., Lemmi C. A., Davidson W. D. Zollinger-Ellison syndrome in a patient with multiple carcinoid-islet cell tumors of the duodenum. Am J Surg. 1968 Feb;115(2):177–184. doi: 10.1016/0002-9610(68)90026-3. [DOI] [PubMed] [Google Scholar]
  40. Trudeau W. L., McGuigan J. E. Relations between serum gastrin levels and rates of gastric hydrochloric acid secretion. N Engl J Med. 1971 Feb 25;284(8):408–412. doi: 10.1056/NEJM197102252840803. [DOI] [PubMed] [Google Scholar]
  41. VENABLE J. H., COGGESHALL R. A SIMPLIFIED LEAD CITRATE STAIN FOR USE IN ELECTRON MICROSCOPY. J Cell Biol. 1965 May;25:407–408. doi: 10.1083/jcb.25.2.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Vassallo G., Capella C., Solcia E. Endocrine cells of the human gastric mucosa. Z Zellforsch Mikrosk Anat. 1971;118(1):49–67. doi: 10.1007/BF00331766. [DOI] [PubMed] [Google Scholar]
  43. Vassallo G., Solcia E., Capella C. Light and electron microscopic identification of several types of endocrine cells in the gastrointestinal mucosa of the cat. Z Zellforsch Mikrosk Anat. 1969;98(3):333–356. doi: 10.1007/BF00346679. [DOI] [PubMed] [Google Scholar]
  44. WILLIAMS E. D., SANDLER M. The classification of carcinoid tum ours. Lancet. 1963 Feb 2;1(7275):238–239. doi: 10.1016/s0140-6736(63)90951-6. [DOI] [PubMed] [Google Scholar]

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