Changes in blood catecholamine levels and ultrastructure of dog adrenal medullary cells during hemorrhagic shock

Virchows Archiv B volume 23, Article number: 1 (1977) Cite this article

Summary

Blood catecholamine levels and ultrastructural changes in adrenal medullary cells were followed during the course of oligemic and normovolemic shock in dogs. Blood adrenaline concentration rose promptly after hemorrhage, reaching a maximum that was 10-fold greater than normal during the early period of hemorrhagic hypotension. Thereafter, adrenaline levels gradually declined until the end of the critical stage of hemorrhagic shock when the blood concentration rose to a level 8-fold that of normal. Following the critical stage, and throughout the irreversible stages of shock, adrenaline levels remained near normal. Noradrenaline, which was initially undetectable, first appeared in the impending stage of hemorrhagic hypotension and showed little change during the course of severe hemorrhagic hypotension.

Ultrastructural studies demonstrated A-cell degranulation as early as 5 min after initiation of hemorrhage. Degranulation continued throughout the impending stage of hemorrhagic hypotension and was associated with an increasing number of autophagic vacuoles containing empty vesicles. At the end of the critical stage, all A cells showed complete degranulation and degenerative hydropic change. Progression to necrosis rather than arrest or reversal of hydropic change was observed after reinfusion of blood. In contrast to the marked alterations in A cells, most N cells were morphologically unchanged.

This is a preview of subscription content, access via your institution.

References

  1. Abrahams, S.J., Holtzman, E.: Secretion and endocytosis in insulin-stimulated rat adrenal medulla cells J. Cell Biol.56, 540–558 (1973)

    PubMed  Article  CAS  Google Scholar 

  2. Al-Ami, F.: Light and electron microscopy of the adrenal medulla ofMacaca mulata monkey. Anat. Rec.164, 317–332 (1969)

    Article  Google Scholar 

  3. Allen, J.M.: The influence of cold, inanition and insulin shock upon the histochemistry of adrenal medulla of the mouse. J. Histochem. Cytochem.4, 341–346 (1956)

    PubMed  CAS  Google Scholar 

  4. Bedford, E.A.: The epinephrine content of the blood in conditions of low blood pressure and shock. Amer. J. Physiol.43, 235–257 (1917)

    Google Scholar 

  5. Benedeczky, I., Smith, A.D.: Ultrastructural studies on the adrenal medulla of golden hamster. Origin and fate of secretory granules. Z. Zellforch.124, 367–386 (1972)

    Article  CAS  Google Scholar 

  6. Brown, W.J., Barajas, L., Latta, H.: The ultrastructure of the human adrenal medulla: with comparative studies of white rat. Anat. Rec.169, 173–184 (1971)

    PubMed  Article  CAS  Google Scholar 

  7. Brundin, T.: Catecholamines in the preaortal paraganglia of fetal rabbits. Acta physiol. scand.64, 287–288 (1965)

    PubMed  CAS  Google Scholar 

  8. Coupland, R.E.: Electron microscopic observations on the structure of the rat adrenal medulla. I. The ultrastructure and organization of chromaffin cells in the normal adrenal medulla. J. Anat. (Lond.)99, 231–254 (1965)

    CAS  Google Scholar 

  9. Coupland, R.E., Hopwood, D.: The mechanism of the differential staining reaction for adrenaline- and noradrenaline-storing granules in tissues fixed in glutaraldehyde. J. Anat. (Lond.)100, 227–243 (1966)

    CAS  Google Scholar 

  10. Coupland, R.E., Pyper, A.S., Hopwood, D.: A method for differentiating between noradrenaline- and adrenaline-storing cells in the light and electron microscope. Nature (Lond.)201, 1240–1242 (1964)

    Article  CAS  Google Scholar 

  11. DeRobertis, E., Sabatini, D.D.: Submicroscopic analysis of the secretory process in the adrenal medulla. Fed. Proc.19, Suppl. 5, 70–78 (1960)

    Google Scholar 

  12. DeRobertis, E., Vaz Ferreira, A.: A multivesicular catechol containing body of the adrenal medulla of the rabbit. Exp. Cell Res.12, 575–581 (1957)

    Article  CAS  Google Scholar 

  13. Douglas, W.W.: Stimulus-secretion coupling. The concept and clues from chromaffin and other cells. Brit. J. Pharmac.34, 451–474 (1968)

    CAS  Google Scholar 

  14. Eränkö, O., Hopsu, V.: Effect of reserpine on the histochemistry and content of adrenaline and noradrenaline in the adrenal medulla of the rat and mouse. Endocrinology62, 15–23 (1958)

    PubMed  Article  Google Scholar 

  15. Greever, C.J., Watts, D.T.: Epinephrine levels in the peripheral blood during irreversible hemorrhagic shock in dogs. Circulat. Res.7, 192–195 (1959)

    PubMed  CAS  Google Scholar 

  16. Grynszpan-Winograd, O.: Morphological aspects of exocytosis in the adrenal medulla. Phil. Trans. B261, 291–292 (1971)

    Article  CAS  Google Scholar 

  17. Hervonen, A., Korkala, O.: Effect of hypoxia on the fine structure of the catecholamine-storing cells of the human fetal paraganglia. Virchows Arch. Abt. B Zellpath.13, 341–349 (1973)

    CAS  Google Scholar 

  18. Heymans, C.: Le sinus carotidien, zone reflexogene regulatrice du tonus vagal cardiaque du tonus neurovasculaire et de l’adrenalino secretion. Arch. internat. Pharmacodyn.35, 269–306 (1929)

    Google Scholar 

  19. Hillarp, N.A., Hökfelt, B.: Evidence of adrenaline and noradrenaline in separate adrenal medullary cells. Acta physiol. scand.30, 55–68 (1953)

    PubMed  CAS  Google Scholar 

  20. Hillarp, N.A., Hökfelt, B.: Histochemical demonstration of noradrenaline and adrenaline in the adrenal medulla. J. Histochem. Cytochem.3, 1–5 (1955)

    PubMed  CAS  Google Scholar 

  21. Hillarp, N.A., Hökfelt, B., Nilson, B.: The cytology of the adrenal medullary cells with special reference to the storage and secretion of the sympathomimetic amines. Acta anat. (Basel)21, 115–167(1954)

    Google Scholar 

  22. Holtzman, E., Teichberg, S., Abrahams, S.J., Citkowitz, E., Crain, S.M., Kawai, N., Peterson, E.R.: Notes on synaptic vesicles, endoplasmic reticulum, lysosomes and peroxisomes in nervous tissue and the adrenal medulla. J. Histochem. Cytochem.21, 349–385 (1973)

    PubMed  CAS  Google Scholar 

  23. Kajihara, H., Hara, H., Seyama, S., Iijima, S., Yoshida, M.: Light and electron microscopic observations of the myocardium of dogs in hemorrhagic shock. Acta path. jap.23, 315–333 (1973)

    PubMed  CAS  Google Scholar 

  24. Lever, J.D., Findlay, J.A.: Similar structural bases for the storage and release of secretory material in adreno-medullary andβ pancreatic cells. Z. Zellforsch.74, 317–324 (1966)

    PubMed  Article  CAS  Google Scholar 

  25. Manger, W.M., Bollman, J.L., Maher, F.T., Berkson, J.: Plasma concentration of epinephrine and norepinephrine in hemorrhagic and anaphylactic shock. Amer. J. Physiol.190, 310–316 (1957)

    PubMed  CAS  Google Scholar 

  26. Mascorro, J.A., Yates, R.D.: Ultrastructural studies of the effects of reserpine on mouse abdominal sympathetic paraganglia. Anat. Rec.170, 169–280 (1971)

    Article  Google Scholar 

  27. Mirkin, B.L.: The effect of synaptic blocking agents on reserpine-induced alterations in adrenal medullary and urinary catecholamine levels. J. Pharm. exp. Ther.133, 34–40 (1961)

    CAS  Google Scholar 

  28. Poole, T.R., Watts, T.: Peripheral blood epinephrine levels in dogs during intravenous infusion. Amer. J. Physiol.196, 145–148 (1959)

    PubMed  CAS  Google Scholar 

  29. Satake, Y.: Amount of epinephrine secreted from suprarenal glands in dogs in hemorrhage, and poisoning with guanidine, caffeine, urethane, camphor, etc. Tohoku J. exp. Med.17, 333–344 (1931)

    Article  Google Scholar 

  30. Stoner, H.B., Marshall, H.W.: Studies on the mechanism of shock. The importance of central catecholaminergic neurons in the response to injury. Brit. J. exp. Path.56, 157–166 (1975)

    PubMed  CAS  Google Scholar 

  31. Tramezzani, J.H., Chiocchio, S., Wassermann, G.F.: A technique for light and electron microscopic identification of adrenaline- and noradrenaline-storing cells. J. Histochem. Cytochem.12, 890–899 (1964)

    PubMed  CAS  Google Scholar 

  32. Wacker, Ph., Forssmann, W.G.: Immersion and perfusion fixed rat adrenal medulla. The problem of mixed cells, clear cells, and the mode of secretion. Z. Zellforsch.126, 261–277 (1972)

    PubMed  Article  CAS  Google Scholar 

  33. Walton, R.P., Richardson, J.A., Walton, R.P., Jr., Thompson, W.L.: Sympathetic influences during hemorrhagic hypotension. Amer. J. Physiol.197, 223–230 (1959)

    PubMed  CAS  Google Scholar 

  34. Watts, D.T.: Arterial blood epinephrine levels during hemorrhagic hypotension in dogs. Amer. J. Physiol.184, 271–274 (1956)

    PubMed  CAS  Google Scholar 

  35. Wetzstein, R.: Elektronenmikroskopische Untersuchungen am Nebennierenmark von Maus, Meerschweinchen und Katze. Z. Zellforsch.46, 517–576 (1957)

    PubMed  Article  CAS  Google Scholar 

  36. Wiggers, C.J.: Myocardial depression in shock. A survey of cardiodynamic studies. Amer. Heart J.33, 633–650 (1947)

    Article  Google Scholar 

  37. Wood, J.G., Barrnett, R.J.: Histochemical demonstration of norepinephrine at a fine structural level. J. Histochem. Cytochem.12, 197–209 (1964)

    PubMed  CAS  Google Scholar 

  38. Zyss, R., Gajkowska, B.: Changes in the function and fine structure of the chromaffin cells of rat adrenal medulla after burn. Pol. med. J.11, 405–414 (1972)

    PubMed  CAS  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Pathology, Research Institute for Nuclear Medicine and Biology, Hiroshima University, 734 Hiroshima-Shi, Kasumi 1-2-3, Japan

    Hiroki Kajihara

  2. Department of Surgery, Hiroshima University School of Medicine, 734 Hiroshima-Shi, Kasumi 1-2-3, Japan

    Shunji Hirata & Nobukazu Miyoshi

Authors
  1. Hiroki Kajihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shunji Hirata
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nobukazu Miyoshi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroki Kajihara.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kajihara, H., Hirata, S. & Miyoshi, N. Changes in blood catecholamine levels and ultrastructure of dog adrenal medullary cells during hemorrhagic shock. Virchows Arch. B Cell Path. 23, 1 (1977). https://doi.org/10.1007/BF02889115

Download citation

Key words

  • A-cell
  • N-cell
  • Degranulation
  • Hydropic change
  • Necrot-ic cell