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Ultrastructural and histological study of 11 bronchial carcinoids

Evidence for different types

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Summary

Seven of eleven bronchial carcinoids investigated showed cells with small granules resembling P cells which have already been described in human fetal and adult lung; two of these P cell tumours showed distinctive paraganglioid features. One tumour showed peculiar ultrastructural findings resembling closely those previously reported by Black (1969) in a so called “pulmonary oncocytoma”. Three remaining cases showed large secretory granules resembling those of type 3 cells already described by Hage (1973 b) in bronchial carcinoids; one of these tumours produced large amounts of 5-hydroxytryptamine (5HT). It is concluded that, on cytological grounds, at least two types of tumours can be distinguished among bronchial carcinoids, i.e. P cell and type 3 cell tumours. Moreover, two varieties of P cell carcinoids have been recognized, showing either the less frequent and more distinctive paraganglioid structure or the more common trabecular structure.

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References

  • Allison, D.J., Clay, T.: Angiotensin II release from the hypoxic lobe of the intact dog lung. J. Physiol. (Lond.) 260, 32P-33P (1976)

    Google Scholar 

  • Basset, F., Poirier, J., Le Crom, M., Turiaf, J.: Etude ultrastructurale de 1'epithelium bronchiolaire humain. Z. Zellforsch. 116, 425–442 (1971)

    Google Scholar 

  • Bearzi, I., Fabris, G., Brugiapaglia, C.: Studio morfologico, istochimico ed ultrastrutturale dei carcinoidi bronchiali. Riv. Patol. Clin. Sper. (Padova) 14, 71–90 (1974)

    Google Scholar 

  • Bensch, K.G., Corrin, B., Pariente, R., Spencer, H.: Oat cell carcinoma of the lung: its origin and relationship to bronchial carcinoid. Cancer 22, 1163–1172 (1968)

    Google Scholar 

  • Bensch, K.G., Gordon, G.B., Miller, L.R.: Studies on the bronchial counterpart of the Kultschitzky (argentaffin) cell and innervation of bronchial glands. J. Ultrastruct. Res. 12, 668–686 (1965a)

    Google Scholar 

  • Bensch, K.G., Gordon, B., Miller, L.R.: Electron microscopic and biochemical studies on the bronchial carcinoid tumor. Cancer 18, 592–602 (1965b)

    Google Scholar 

  • Berkov, S.: Hypoxic pulmonary vasoconstriction in the rat. The necessary role of angiotensin II. Circulation Res. 35, 256–261 (1974)

    Google Scholar 

  • Black, W.C.: Pulmonary oncocytoma. Cancer 23, 1347–1357 (1969)

    Google Scholar 

  • Bonikos, D.S., Archibald, R., Bensch, K.G.: On the origin of the so-called tumorlets of the lung. Human Path. 7, 461–469 (1967 a)

    Google Scholar 

  • Bonikos, D.S., Bensch, K.G., Jamplis, R.W.: Peripheral pulmonary carcinoid tumors. Cancer 37, 1977–1998 (1976 b)

    Google Scholar 

  • Brune, J., Saubier, E., Colobert, L., Guidollet, J., Galy, P.: Carcinoidose par métastases hépatiques d'une tumeur bronchique opérée trois ans auparavant. Rev. Fr. Mal. Resp. 1, 377–386 (1973)

    Google Scholar 

  • Canepa, M., Carli, C., Barbieri, A.: Studio al microscopio elettronico dell'adenoma bronchiale carcinoide. Pathologica (Genova) 61, 345–352 (1969)

    Google Scholar 

  • Capella, C., Bordi, C., Monga, G., Buffa, R., Fontana, P., Bonfanti, S., Bussolati, G., Solcia, E.: Multiple endocrine cells in thyroid medullary carcinoma. Evidence for calcitonin, somatostan, ACTH, 5HT, and small granule cells. Virchows Arch. A Path. Anat. and Histol. 377, 111–128 (1978a)

    Google Scholar 

  • Capella, C., Hage, E., Solcia, E., Usellini, L.: Ultrastructural similarity of endocrine-like cells of the human lung and some related cells of the gut. Cell Tiss. Res. 186, 25–37 (1978b)

    Google Scholar 

  • Capella, C., Solcia, E., Frigerio, B., Buffa, R., Usellini, L., Fontana, P.: The endocrine cells of the pancreas and related tumours. Ultrastructural study and classification. Virchows Arch. A Path. Anat. Histol. 373, 327–352 (1977)

    Google Scholar 

  • Churg, A., Warnock, M.L.: Pulmonary tumorlet. A form of peripheral carcinoid. Cancer (Philad.) 37, 1469–1477 (1976)

    Google Scholar 

  • Cutz, E., Chan, W., Wong, V., Conen, P.E.: Endocrine cells in rat fetal lungs. Ultrastructural and histochemical study. Lab. Invest. 30, 458–464 (1974)

    Google Scholar 

  • Ericson, L.E., Hakanson, R., Larson, B., Owman, Ch., Sundler, F.: Fluorescence and electron microscopy of amine-storing enterochromaffin-like cells in tracheal epithelium of mouse. Z. Zellforsch. 124, 532–545 (1972)

    Google Scholar 

  • George, J.M., Capen, C.C., Phillips, A.S.: Biosynthesis of vasopressin in vitro and ultrastructure of a bronchialgenic carcinoma. J. Clin. Invest. 51, 141–148 (1972)

    Google Scholar 

  • Gewirtz, G., Yalow, R.S.: Ectopic-ACTH production in carcinoma of the lung. J. Clin. Invest. 53, 1022–1032 (1974)

    Google Scholar 

  • Gmelich, J.T., Bensch, K.G., Liebow, A.A.: Cells of Kultschitzky type in bronchioles and their relation to the origin of peripheral carcinoid tumor. Lab. Invest. 17, 88–98 (1967)

    Google Scholar 

  • Grimelius, L.: A silver nitrate stain for α 2 cells in human pancreatic islets. Acta Soc. Med. uppsalien. 73, 243–270 (1968)

    Google Scholar 

  • Hage, E.: Electron microscopic identification of several types of endocrine cells in the bronchial epithelium of human foetuses. Z. Zellforsch. 141, 401–412 (1973a)

    Google Scholar 

  • Hage, E.: Histochemistry and fine structure of bronchial carcinoid tumours. Virchows Arch. Abt. A Path. Anat. 361, 121–128 (1973b)

    Google Scholar 

  • Hage, E.: Endocrine-like cells of the pulmonary epithelium. In: Chromaffin, Enterochromaffin and Related Cells (R.E. Coupland and T. Fujita, eds.) pp. 317–332. Amsterdam: Elsevier 1976

    Google Scholar 

  • Hage, E., Hage, J., Juel, G.: Endrocrine-like cells of the pulmonary epithelium of the human adult lung. Cell Tiss. Res. 178, 39–48 (1977)

    Google Scholar 

  • Hattori, S., Matsuda, M., Tatseishi, R., Nishihara, H., Horai, T.: Oat-cell carcinoma of the lung. Cancer 30, 1014–1024 (1972)

    Google Scholar 

  • Horvath, E., Kovacs, K.: Morphogenesis and significance of fibrous bodies in human pituitary adenomas. Virchows Arch. B Cell Path. 27, 69–78 (1978)

    Google Scholar 

  • Hosoda, S., Nakamura, W., Suzuki, H., Hoshino, M., Karasawa, K.: A bronchial carcinoid having low serotonin concentration. Arch. Path. 90, 320–324 (1970)

    Google Scholar 

  • Imura, H., Matsukura, S., Yamamoto, H., Hirata, Y., Nakai, Y., Endo, J., Tanaka, A., Nakamura, M.: Studies on ectopic ACTH-producing tumors. II. Clinical and biochemical features of 30 cases. Cancer 35, 1430–1437 (1975)

    Google Scholar 

  • Lauweryns, J.M., Cokelaere, M., Theunynck, P.: Neuroepithelial bodies in the respiratory mucosa of various mammals. A light optical, histochemical and ultrastructural investigation. Z. Zellforsch. 135, 569–592 (1972)

    Google Scholar 

  • Lauweryns, J.M., Cokelaere, M., Theunynck, P.: Serotonin producing neuro-epithelial bodies in rabbit respiratory mucosa. Science 180, 410–413 (1973)

    Google Scholar 

  • Lauweryns, J.M., Peuskens, J.C.: Neuro-epithelial bodies (Neuroreceptor or secretory organs?) in human infant bronchial and bronchiolar epithelium. Anat. Rec. 172, 471–482 (1972)

    Google Scholar 

  • McDonald, D.M., Mitchell, R.A.: The innervation of glomus cells, ganglion cells and blood vessels in the rat carotid body: a quantitative ultrastructural analysis. J. Neurocytol. 4, 177–230 (1975)

    Google Scholar 

  • Pariente, R., Even, P., Brouet, G.: Etude ultrastructurale des carcinoïdes bronchiques. Press. Med. 75, 183–188 and 221–224 (1967)

    Google Scholar 

  • Patchefsky, A.S., Gordon, G., Herrer, W.V., Hoch, W.S.: Carcinoid tumor of the pancreas. Ultrastructural observations of a lymph node metastasis and comparison with bronchial carcinoid. Cancer 33, 1349–1354 (1974)

    Google Scholar 

  • Pearse, A.G.E.: Histochemistry, theoretical and applied. Vol. 1. London: Churchill 1968

    Google Scholar 

  • Picardi, C., Picardi, R., Tonelli, F.: Biochemical and ultrastructural study on bronchial carcinoids. Tumori 58, 129–136 (1972)

    Google Scholar 

  • Ratcliffe, J.G., Scott, A.P., Bennett, H.P.J., Lowry, P.J., McMartin, C., Strong, J.A., Walbaum, P.R.: Production of a corticotrophin-like intermediate lobe peptide and of corticotrophin by a bronchial carcinoid tumour. Clin. Endocrinol. 2, 51–55 (1973)

    Google Scholar 

  • Rosai, J., Levine, G.D.: Tumors of the thymus. In: Atlas of tumor pathology. Fasc. 13. Washington: Armed Forces Institute of Pathology 1976

    Google Scholar 

  • Said, S.I.: Endocrine role of the lung in disease. Am. J. Med. 57, 453–465 (1974)

    Google Scholar 

  • Said, S.I., Mutt, V.: Long acting vasodilator peptide from lung tissues. Nature 224, 699–700 (1969)

    Google Scholar 

  • Said, S.I., Mutt, V.: Relationship of spasmogenic and smooth muscle relaxant peptides from normal lung to other vasoactive compounds. Nature 265, 84–86 (1977)

    Google Scholar 

  • Sevier, A.C., Munger, B.L.: A silver method for paraffin sections of neural tissue. J. Neuropathol. exp. Neurol. 24, 130–135 (1965)

    Google Scholar 

  • Sing, G., Lee, R.E., Brooks, D.H.: Primary pulmonary paraganglioma. Report of a case and review of the literature. Cancer 40, 2286–2289 (1977)

    Google Scholar 

  • Soga, J., Tazawa, K., Sano, M., Kohro, T., Morooka, H., Karaki, Y., Takahashi, S.: Analysis of carcinoid granules in relation to a recent concept of carcinoids as endocrine neoplasms of the primitive gut system. Acta Path. Jap. 25, 707–716 (1975)

    Google Scholar 

  • Solcia, E., Capella, C., Vassallo, G.: Lead-haematoxylin as a stain for endocrine cells. Significance of staining and comparison with other selective methods. Histochemie 20, 116–126 (1969a)

    Google Scholar 

  • Solcia, E., Capella, C., Vassallo, G., Buffa, R.: Endocrine cells of the gastric mucosa. Internat. Rev. Cytol. 42, 223–286 (1975)

    Google Scholar 

  • Solcia, E., Sampietro, R., Capella, C.: Differential staining of catecholamines, 5-hydroxytryptamine and related compounds in aldehyde-fixed tissues. Histochemie 17, 273–283 (1969 b)

    Google Scholar 

  • Sönksen, P.H., Ayres, A.B., Braimbridge, M., Corrin, B., Davies, D.R., Jeremiah, G.M., Oaten, S.W., Lowy, C., West, T.E.T.: Acromegaly caused by pulmonary carcinoid tumours. Clin. Endocrinol. 5, 503–513 (1976)

    Google Scholar 

  • Terzakis, J.A., Sommers, S.C., Andersson, B.: Neurosecretory appearing cells of human segmental bronchi. Lab. Invest. 26, 127–132 (1972)

    Google Scholar 

  • Upton, G.V., Amatruda, T.T.: Evidence for the presence of tumor peptides with corticotrophinreleasing-factor-like activity in the ectopic ACTH syndrome. New Engl. Med. 285, 419–424 (1971)

    Google Scholar 

  • Vassallo, G., Capella, C., Solcia, E.: Grimelius' silver stain for endocrine cell granules, as shown by electron microscopy. Stain Technol. 46, 7–13 (1971)

    Google Scholar 

  • Verley, J.M.: Les tumeurs carcinoïdes bronchiques et digestives de l'homme. Z. Krebsforsch. 66, 503–516 (1965)

    Google Scholar 

  • Vorherr, H., Massry, S.G., Fallet, R., Kaplan, L., Kleeman, C.R.: Antidiuretic principle in tuberculous lung tissue of a patient with pulmonary tuberculosis and hyponatremia. Ann. Int. Med. 72, 383–387 (1970)

    Google Scholar 

  • Wharton, J., Polak, J.M., Bloom, S.R., Ghatei, M.A., Solcia, E., Brown, M.R., Pearse, A.G.E.: Bombesin-like immunreactivity in the lung. Nature 273, 769–770 (1978)

    Google Scholar 

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Supported in part by grants N. 76.01558.04 and 77.01252.04 from the Italian Research Council (C.N.R.)

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Capella, C., Gabrielli, M., Polak, J.M. et al. Ultrastructural and histological study of 11 bronchial carcinoids. Virchows Arch. A Path. Anat. and Histol. 381, 313–329 (1979). https://doi.org/10.1007/BF00432474

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