Abstract
Electrical stimulation of a single cervical vagus nerve produces neurogenic inflammation on the stimulated side of the bronchial tree, including the first (main) to the 4th order bronchi. In the contralateral bronchial tree, in contrast, only the proximal part of the main bronchus exhibits inflammatory changes, suggesting that vagal sensory axons present in the bronchi largely originate from the ipsilateral vagus nerve. Intravenous administration of capsaicin can evoke neurogenic inflammation in bilateral bronchial trees. Sensory axons from various sources are thought to be stimulated by this irritant. The extent to which neurogenic inflammation in both bronchial trees might be reduced by unilateral vagotomy is not known. In the present study, we sought to characterize the effect of unilateral cervical vagotomy on capsaicin-induced changes in plasma extravasation and secretory activity of goblet cells in the bronchial trees of both sides. To quantify the magnitude of neurogenic plasma extravasation, Evans blue was used as a tracer dye to measure spectrophotometrically its amount in the bronchial wall. Another tracer dye, Monastral blue, was used to localize the distribution of leaky blood vessels and to measure morphometrically their area density in the whole mounts. To investigate cell and tissue responses of the mucosa, histological methods were employed. After 2 or 4 postoperative weeks, the rats were intravenously administered with a single dose of capsaicin, 150 μg/kg. This resulted in different magnitudes of Evans blue extravasation in the bronchi of the two sides in vagotomized rats. Extravasation of Evans blue dye in the bronchial tree ipsilateral to vagotomy was one-half to two-thirds of that of the contralateral bronchial tree. For the distal region of the main stem bronchus, the area density of Monastral blue-labeled blood vessels in the operated side was one-half of that in the unoperated side, and for the secondary bronchus, the area density of these blood vessels in the operated side was one-quarter of that in the unoperated side. Histological study indicated that in the bronchial mucosa ipsilateral to vagotomy edematous change was not obvious, and most goblet cells were not responsive to stimulation by capsaicin, in contrast to the contralateral side where edematous change was very prominent and goblet cells were very sensitive to capsaicin. It is concluded that unilateral cervical vagotomy could selectively desensitize the mucosa of the ipsilateral bronchial tree to capsaicin, and therefore, decrease the magnitude of neurogenic inflammation.
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References
Bałuk P, Gabella G (1989) Innervation of the guinea pig trachea: a quantitative morphological study of intrinsic neurons and extrinsic nerves. J Comp Neurol 285:117–132
Bałuk P, Nadel JA, McDonald DM (1992) Substance P-immunoreactive sensory axons in the respiratory tract: a quantitative study of their distribution and role in neurogenic inflammation. J Comp Neurol 319:586–598
Bancroft JD, Stevens A (1982) Theory and practice of histological techniques. 2nd edn. Churchill Livingstone, Edinburgh
Boschetto P, Rogers DF, Fabbri LM, Barnes PJ (1991) Corticosteroid inhibition of airway microvascular leakage. Am Rev Respir Dis 143:605–609
Brokaw JJ, McDonald DM (1988) Neurally-mediated increase in vascular permeability in the rat trachea: onset, duration, and tachyphylaxis. Exp Lung Res 14:757–767
Cadieux A, Springall DR, Mulderry PK, Rodrigo J, Ghatei MA, Terenghi G, Bloom SR, Polak JM (1986) Occurrence, distribution and ontogeny of CGRP immunoreactivity in the rat lower respiratory tract: effect of capsaicin treatment and surgical denervation. Neuroscience 19:605–627
Dahlqvist A, Carlsoo B, Hellstrom S, Domeij S, Kourtopoulos H (1986) Fiber composition of the recurrent laryngeal nerve after experimental vagotomy and sympathectomy. Acta Anat 125:114–120
Dalsgaard CJ, Lundberg JM (1984) Evidence for a spinal afferent innervation of the guinea-pig lower respiratory tract as studied by the horseradish peroxidase technique. Neurosci Lett 45:117–122
Huang HT, Haskell A, McDonald DM (1989) Changes in epithelial secretory cells and potentiation of neurogenic inflammation in the trachea of rats with respiratory infections. Anat Embryol 180:325–341
Huang HT, Liu KM, Her WY, Chiang CY (1990) Effect of unilateral vagotomy on capsaicin-induced neurogenic inflammation in the trachea of rats. Kaohsiung J Med Sci 6:461–466
Jancso G, Kiraly E, Jancso-Gabor A (1977) Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. Nature 270:741–743
Jeffery PK, Reid L (1975) New observations of rat airway epithelium: a quantitative and electron microscopic study. J Anat 120:295–320
Kou H-P, Rohde JAL, Tokuyama K, Barnes PJ, Rogers DF (1990) Capsaicin and sensory neuropeptide stimulation of goblet cell secretion in guinea-pig trachea. J Physiol (Lond) 431:629–641
Lamb D, Reid L (1969) Histochemical types of acidic glycoprotein produced by mucous cells of the tracheobronchial glands in man. J Pathol 98:213–229
Ling EA, Wong WC (1988) An electron microscopic study of the nodose (inferior vagal) ganglion cells in the monkey. J Neurocytol 17:845–857
Lundberg JM, Saria A (1983) Capsaicin-induced desensitization of airway mucosa to cigarette smoke, mechanical and chemical irritants. Nature 302:251–253
Lundberg JM, Brodin E, Saria A (1983a) Effects and distribution of vagal capsaicin-sensitive substance P neurons with special reference to the trachea and lungs. Acta Physiol Scand 119:243–252
Lundberg JM, Saria A, Martling CR (1983b) Capsaicin pretreatment abolishes cigarette smoke-induced oedema in rat tracheobronchial mucosa. Eur J Pharmacol 86:317–318
Lundberg JM, Hokfelt 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
McDonald DM (1988a) Neurogenic inflammation in the rat trachea. I. Changes in venules, leukocytes, and epithelial cells. J Neurocytol 17:583–603
McDonald DM (1988b) Respiratory tract infections increase susceptibility to neurogenic inflammation in the rat trachea. Am Rev Respir Dis 137:1432–1440
McDonald DM, Mitchell RA, Gabella G, Haskell A (1988) Neurogenic inflammation in the rat trachea. II. Identity and distribution of nerves mediating the increase in vascular permeability. J Neurocytol 17:605–628
McDonald DM, Schoeb TR, Lindsey JR (1991) Mycoplasma pulmonis infections cause long-lasting potentiation of neurogenic inflammation in the respiratory tract of the rat. J Clin Invest 87:787–799
Piedimonte G, McDonald DM, Nadel JA (1990) Glucocorticoids inhibit neurogenic plasma extravasation and prevent viruspotentiated extravasation in the rat trachea. J Clin Invest 86:1409–1415
Saria A, Lundberg JM (1983) Evans blue fluorescence: quantitative and morphological evaluation of vascular permeability in animal tissues. J Neurosci Methods 8:41–49
Saria A, Martling C-R, Dalsgaard C-J, Lundberg JM (1985) Evidence for substance P-immunoreactive spinal afferents that mediate bronchoconstriction. Acta Physiol Scand 125:407–414
Schoeb TR, Lindsey JR (1987) Exacerbation of murine respiratory mycoplasmosis by sialodacryoadenitis virus infection in gnotobiotic F344 rats. Vet Pathol 24:392–399
Schoeb TR, Kervin KC, Lindsey JR (1985) Exacerbation of murine respiratory mycoplasmosis in gnotobiotic F344/N rats by Sendai virus infection. Vet Pathol 22:272–282
Tokuyama K, Kuo H-P, Rohde JAL, Barnes PJ, Rogers DF (1990) Neural control of goblet cell secretion in guinea pig airways. Am J Physiol 259:L108-L115
Umeno E, Nadel JA, Huang HT, McDonald DM (1989) Inhibition of neutral endopeptidase potentiates neurogenic inflammation in the rat trachea. J Appl Physiol 66:2647–2652
Umeno E, Nadel JA, McDonald DM (1990) Neurogenic inflammation of the rat trachea: fate of neutrophils that adhere to venules. J Appl Physiol 69:2131–2136
Weibel E (1979) Stereological Methods, vol 1. Practical Methods for Biological Morphometry. Academic Press, London
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Huang, HT. Unilateral cervical vagotomy decreases the magnitude of neurogenic inflammation induced by capsaicin in the ipsilateral bronchial tree of rats. Anat Embryol 188, 363–370 (1993). https://doi.org/10.1007/BF00185945
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DOI: https://doi.org/10.1007/BF00185945