Summary
In order to clarify the early phenomena involved in the lung reaction to hyperoxia, twenty adult male rats were exposed to 100% oxygen at 1 ATA. Morphological pulmonary lesions were detectable after only 24 h hyperoxia, and included vasoconstriction and perivascular oedema, bronchiolar constriction, and pericyte reaction. The lesions were irregularly scattered within the lung parenchyma and occurred preferentially in areas centred on bronchiolo-vascular stems. Even at the latest stages, pulmonary heterogeneity was obvious, from the coexistence of areas damaged at different times. Neuro-epithelial-bodies were found under the bronchiolar epithelium; the morphological aspect of the neuro-endocrine cells observed was consistent with hyperoxia-induced modulation of their secretory activity. Taken together, our findings show the speed of development of hyperoxia-induced pulmonary changes and raise some pathogenic considerations.
Similar content being viewed by others
References
Ainsworth DM, Keith IM, Lobas JG, Farrell PM, Eicker SW (1986) Oxygen toxicity in the infant rhesus monkey lung. Light microscopic and ultrastructural studies. Histol Histo Pathol 1:75–87
Balentine JD (1982) Principles of hyperoxic pathophysiology. In: Balentine JD (ed) Pathology of oxygen toxicity. Academic Press, New York, pp 31–81
Bitterman PB, Wewers MD, Rennard SI, Adelberg S, Crystal RG (1986) Modulation of alveolar macrophage - driven fibroblast proliferation by alternative macrophage mediators. J Clin Invest 77:700–708
Block ER, Stalcup SA (1981) Depression of serotonin uptake by cultured endothelial cells exposed to high O2 tensions. J Appl Physiol 50:1212–1215
Castairs JR, Barnes PJ (1986) Autoradiographic mapping of substance P receptors in lung. Eur J Pharmacol 127:295–296
Claman HN (1987) Mast-cells and immunologically mediated fibrosis. In: Revillard JP, Wierzbicki N (eds) Tissue fibrosis: immune cells and mediators. Local Immunity. Suresne (Fondation Franco-Allemande), Vol 3, pp 84–97
Crapo JD, Tierney DF (1974) Superoxide dismutase and pulmonary oxygen toxicity. Am J Physiol 226:1401–1407
Crystal RG (1974) Lung collagen: definition, diversity and development. Fed Proc 33:2248–2255
Crystal RG, Bitterman PB, Rennard SI, Hance AJ, Keogh BA (1984) Interstitial lung diseases of unknown cause: disorders characterized by chronic inflammation of the lower respiratory tract. N Engl J Med 310:154–166, 235-244
Davis WB, Rennard SI, Bitterman PB, Crystal RG (1983) Pulmonary oxygen toxicity. Early reversible changes in human alveolar structures induced by hyperoxia. N Engl J Med 309:878–883
D'Orleans-Juste P, Dion S, Drapeau G, Regoli D (1985) Different receptors are involved in the endothelium-mediated relaxation and the smooth muscle contraction of the rabbit pulmonary artery in response to substance P and related neurokinins. Eur J Pharmacol 125:37–44
Garcia JG, Noonan TC, Jubiz W, Malik AB (1987) Leukotrienes and the pulmonary micro-circulation. Ann Rev Resp Dis 136:161–169
Gattinoni L, Pesenti A (1987) ARDS: the non-homogeneous lung; facts and hypothesis. Intensive et Critical Care Digest 6:1–4
Gutner GH, Farrukh IS, Adkinson WF, Sciuto AM, Jacobson JM, Michael JR (1987) The role of arachidonate mediators in peroxide-induced lung injury. Am Rev Resp Dis 136:480–483
Halliwell B (1978) Biochemical mechanisms accounting for the toxic action of oxygen on living organisms: the key role of superoxide dismutase. Cell Biol Int Rep 2:113–128
Hammond B, Kontos HA, Hess ML (1984) Oxygen radicals in adult respiratory distress syndrome, in myocardial ischemia and reperfusion injury, and in cerebral vascular damage. Can J Physiol Pharmacol 63:173–187
Harrison G, Rosan R, Sloane A (1970) Bronchiolitis induced by experimental acute and chronic oxygen intoxication in young adult rats. J Pathol 102:115–122
Heldin CH, Westermark B (1984) Growth factors: mechanism of action and relation to oncogens. Cell 37:9–20
Hess ML, Manson NH (1984) Molecular oxygen: friend and foe. The role of the oxygen-free radical system in the calcium paradox and ischemia/reperfusion injury. J Mol Cell Cardiol 16:969–985
Hill DJ, Strain AJ, Elston SF, Swenne I, Milner RDG (1986) Bifunctional action of transforming growth factor-B on DNA synthesis in early passage human fetal fibroblasts. J Cell Physiol 128:322–328
Housset B, Ody C, Rubin DB, Elemer G, Junod AF (1983) Oxygen toxicity in cultured aortic endothelium: selenium induced partial protective effect. J Appl Physiol 10:343–352
Hua X, Theodrosson-Norhem E, Brodin E, Lundberg JM, Hokfelt T (1985) Multiple tachykinins (neurokinin A, neuropeptide K and substance P) in capsaicin-sensitive sensory neurons in the guinea pig. Reg Pept 13:1–19
James R, Bradshaw RA (1984) Polypeptide growth factors. Annu Rev Biochem 53:259–292
Jamieson D, Chance B, Cadenas E, Boveris A (1986) The relation of free radical production to hyperoxia. Ann Rev Physiol 48:703–719
Jeffery P, Reid L (1972) Intra-epithelial nerves in normal rat airways: a quantative electron microscopic study. J Anat 114:35–45
Kapanci Y, Weibel ER, Kaplan HP, Robinson FR (1969) Pathogenesis and reversibility of the pulmonary lesions of oxygen toxicity in monkeys. II Ultrastructural and morphologic studies. Lab Invest 20:101–106
Kimball RE, Reddy K, Peirce TH, Schwartz LW, Mustafa MG, Cross CE (1976) Oxygen toxicity: augmentation of antioxidant defense mechanisms in rat lung. Am J Physiol 230:1425–1431
Kistler GS, Caldwell PRB, Weibel ER (1967) Developmeut of fine structural damage to alveolar and capillary lining cells in oxygen-poisoned rat lungs. J Cell Biol 32:605–628
Ko SD, Page RC, Narayaran AS (1977) Fibroblast heterogeneity and prostaglandin regulation of subpopulations. Proc Natl Acad Sci USA 74:3429–3432
Lauweryns JM, de Bock V, Guelinckx P, Decramer M (1983) Effects of unilateral hypoxia on neuro-epithelial bodies in rabbit lungs. J Appl Physiol Respir Environ Exercise Physiol 55:1665–1668
Lauweryns JM, Van Lommel A (1986) Effect of various vagotomy procedures on the reaction to hypoxia of rabbit neuro-epithelial bodies: modulation by intra pulmonary axon reflexes? Exp Lung Res 11:319–339
Lundberg JM, Hökfelt T, Martling CR, Saria A, Cuello C (1984) Substance P-immunoreactive sensory nerves in the lower respiratory tract of various mammals including man. Cell Tissue Res 235:251–261
Martinet Y, Crystal RG (1987) Pathogenesis of tissue fibrosis: inflammatory cell modulation of mesenchymental cell accumulation. In: Revillard JP, Wierzbicki N (eds) Tissue fibrosis: immune cells and mediators. Local Immunity. Suresne (Fondation Franco-Allemande), Vol 3, pp 13–31
McCord JM, Wong K (1979) Phagocyte-produced free radicals: roles in cytotoxicity and inflammation. In: Oxygen-free radicals and tissue damage (Ciba Foundation Symposium 65). Excerpta Medica, New York, pp 343–360
Nash G, Blennerhassett JB, Pontoppidan H (1967) Pulmonary lesions associated with oxygentherapy and artificial ventilation. N Engl J Med 276:368–374
Obara H, Sekimoto M, Iwai S (1979) Alterations to the bronchial and bronchiolar surfaces of adult mice after exposure to high concentration of oxygen. Thorax 34:479–485
Pack RJ, Widdicombe JG (1984) Amine-containing cells of the lung. Eur J Resp Dis 65:559–578
Polak JM, Bloom SR (1986) Localization of neural and endocrine peptides. In: Moody TW (ed) Neural and endocrine peptides and receptors. Plenum Press, New York, pp 463–483
Porte A, Stoeckel ME, Mantz JM, Tempé JD, Jaeger A, Batzenschlager A (1978) Acute interstitial pulmonary fibrosis. Comparative light and electron microscopic study of 19 cases. Pathogenic and therapeutic implications. Intens Care Med 4:181–191
Pratt PC (1958) Pulmonary capillary proliferation induced by oxygen inhalation. Am J Pathol 34:1033–1049
Pryor WA (1986) Oxy-radicals and related species: their formation, life-times and reactions. Ann Rev Physiol 48:652–667
Ryan JW (1982) Processing of endogenous polypeptides by the lungs. Ann Rev Physiol 44:241–255
Ryan US (1982) Structural bases for metabolic activity (respiratory physiology). Ann Rev Physiol 44:223–239
Ryan US (1986) Metabolic activity of pulmonary endothelium: modulations of structure and function. Ann Rev Physiol 48:263–277
Said SI (1982) Pulmonary metabolism of prostaglandins and vasoactive peptides. Ann Rev Physiol 44:257–268
Saria A, Martling CR, Theodorsson-Norheim E, Gamse R, Hua XY, Lundberg JM (1987) Coexisting peptides in capsaicin-sensitive sensory neurons: release and actions in the respiratory tract of the guinea-pig. Acta Physiol Hung 69:421–424
Shepro D, Dunham B (1986) Endothelial cell metabolism of biogenic amines. Ann Rev Physiol 48:335–345
Ward P (1986) Oxygen radicals and microvascular injury of lungs and kidneys. Acta Physiol Scand suppl 548:79–85
Wharton J, Polak JM, Bloom SR, Will JA, Rush MR, Pearse AGE (1979) Substance P-like immunoreactive nerves in mammalian lung. Invest Cell Pathol 2:3–10
Will JA (1982) Neuroendocrine and metabolic factors in pulmonary circulatory control. Adv Shock Res 8:13–20
Widdicombe JG (1981) Nervous receptors in the respiratory tract and lungs. In: Hornbein T (ed) Lung biology in health and disease. Vol 17 part I, Regulation of Breathing. Dekker, New York, pp 429–472
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Porte, A., Mantz, J., Hindelang, C. et al. Early bronchopulmonary lesions in rat lung after normobaric 100% oxygen exposure and their evolution. Vichows Archiv A Pathol Anat 414, 135–145 (1989). https://doi.org/10.1007/BF00718593
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00718593