Abstract
The enteric nervous system appears to play a pivotal role in the functional recovery of the gastrointestinal tract after partial resection and reanastomosis, but the structural changes following surgery are not fully understood. The present study was designed to clarify the processes of myenteric plexus regeneration up to one year after transection and reanastomosis of the ileum of the guinea pig. The following techniques were used: nicotinamide adenine dinucleotide (NADH) diaphorase histochemistry, immunostaining of neuron-specific enolase (NSE) in whole-mount preparations, and transmission electron microscopy. Two months after transection and reanastomosis, myenteric ganglion cells with NADH diaphorase reactions were scarce in the center of the lesion, and were less numerous in adjacent areas (3 mm in width) than in the control ileum. In the areas adjacent to the lesion, a few large extraganglionic neurons that did not completely compensate for the loss of ganglion neurons were observed. The remaining ileum showed no changes in NADH diaphorase staining pattern at this stage. Two to 12 months after transection and reanastomosis, ectopic large neurons gradually increased in number not only in the areas adjacent to the lesion but also in part of the remaining ileum, up to 10 cm from the lesion. Concomitantly, large ganglion neurons decreased in number in these areas. In other ileal regions (more than 10 cm distant from the site of transection), no obvious changes in NADH diaphorase staining were noted throughout the observation period. The outgrowth of NSE-containing nerve fibers from the severed stumps was seen two weeks after transection. Six weeks later, numerous bundles of fine nerve fibers with NSE were shown to interconnect the oral and anal cut ends of the myenteric plexus, but they exhibited no subsequent alterations. Transmission electron microscopy revealed that regenerating nerve fiber bundles appeared initially among irregularly arranged smooth muscle cells eight weeks after the operation, as expected from light-microscopic observations. These findings suggest that myenteric ganglion cell bodies, unlike myenteric nerve fibers, require a longer term of reconstruction than previously believed after transection and reanastomosis of the ileum of the guinea pig.
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References
Costa M, Furness JB (1983) The origins, pathways and terminations of neurons with VIP-like immunoreactivity in the guinea-pig small intestine. Neuroscience 8:665–676
Costa M, Furness JB (1989) Structure and neurochemical organization of the enteric nervous system. In: Schultz SG, Makhlout GM, Rauner BB (eds) Handbook of physiology, section 6, vol II. Oxford University Press, Bethesda, Maryland, pp 97–109
Costa M, Buffa R, Furness JB, Solcia E (1980a) Immunohistochemical localization of polypeptides in peripheral autonomic nerves using whole mount preparations. Histochemistry 65:157–165
Costa M, Furness JB, Llewellyn Smith IJ (1980b) An immunohistochemical study of the projections of somatostatin-containing neurons in the guinea-pig intestine. Neuroscience 5:841–852
Costa M, Furness JB, Yanaihara N, Yanaihara C, Moody TW (1984) Distribution and projections of neurons with immunoreactivity for both gastrin-releasing peptide and bombesin in the guinea-pig small intestine. Cell Tissue Res 235:285–293
Daniel EE, Furness JB, Costa M, Belbeck L (1987) The projections of chemically identified nerve fibers in canine ileum. Cell Tissue Res 247:377–384
Dogiel AS (1896) Zwei Arten sympathischer Nervenzellen. Anat Anz 11:679–689
Dogiel AS (1899) Über den Bau der Ganglien in den Geflechten des Darmes und der Gallenblase des Menschen und der Säugethiere. Arch Anat Physiol, Leipzig, Anat Abteil, Jahrgang 130–158
Earlam RJ (1971) Ganglion cell changes in experimental stenosis of the gut. Gut 12:393–398
Ekblad E, Winther C, Ekman R, Håkanson R, Sundler F (1987) Projections of peptide-containing neurons in rat small intestine. Neuroscience 20:169–188
Ekblad E, Ekman R, Håkanson R, Sundler F (1988) Return of nerve fibers containing gastrin-releasing peptide in rat small intestine after local removal of myenteric ganglia. Neuroscience 24:309–319
Endo Y, Uchida T, Kobayashi S (1986) Somatostatin neurons in the small intestine of the guinea pig: a light and electron microscopic immunocytochemical study combined with nerve lesion experiments by laser irradiation. J Neurocytol 15:725–731
Furness JB, Costa M (1971) Monoamine oxidase histochemistry of enteric neurons in the guinea-pig. Histochemie 28:324–336
Furness JB, Costa M (1982) Neurons with 5-hydroxytryptamine-like immunoreactivity in the enteric nervous system: their projections in the guinea-pig small intestine. Neuroscience 7:341–349
Furness JB, Costa M (1987) Studies of neural circuitry of the enteric nervous system. In: The enteric nervous system. Churchill Livingstone, Edinburgh London Melbourne, pp 111–136
Furness JB, Costa M, Miller RJ (1983) Distribution and projections of nerves with enkephalin-like immunoreactivity in the guinea-pig small intestine. Neuroscience 8:653–664
Furness JB, Trussell DC, Pompolo S, Bornstein JC, Smith TK (1990) Calbindin neurons of the guinea-pig small intestine: quantitative analysis of their numbers and projections. Cell Tissue Res 260:261–272
Gabbiani G (1981) The myofibroblast: a key cell for wound healing and fibrocontractive diseases. In: Deyl Z, Milan A (eds) Connective tissue research: chemistry, biology, and physiology. Liss, New York, pp 183–194
Gabella G (1971) Neuron size and number in the myenteric plexus of the newborn and adult rat. J Anat 109:81–95
Gabella G (1984a) Size of neurons and glial cells in the enteric ganglia of mice, guinea-pigs, rabbits and sheep. J Neurocytol 13:49–71
Gabella G (1984b) Size of neurons and glial cells in the intramural ganglia of the hypertrophic intestine of the guinea-pig. J Neurocytol 13:73–84
Gabella G (1987) The number of neurons in the small intestine of mice, guinea-pigs and sheep. Neuroscience 22:737–752
Gabella G (1989) Fall in the number of myenteric neurons in aging guinea pigs. Gastroenterology 96:1487–1493
Galligan JJ, Furness JB, Costa M (1989) Migration of the myoelectric complex after interruption of the myenteric plexus: intestinal transection and regeneration of enteric nerves in the guinea pig. Gastroenterology 97:1135–1146
Gershon MD, Epstein ML, Hegstrand L (1980) Colonization of the chick gut by progenitors of enteric serotonergic neurons: distribution, differentiation, and maturation within gut. Dev Biol 77:41–51
Heppell J, Kelly KA, Sarr MG (1983) Neural control of canine small intestinal interdigestive myoelectric complexes. Am J Physiol 244:G95-G100
Jessen KR, Saffrey MJ, Burnstock G (1983) The enteric nervous system in tissue culture. I. Cell types and their interactions in explants of the myenteric and submucous plexuses from guinea pig, rabbit and rat. Brain Res 262:17–35
Jew JY, Williams TH, Gabella G, Zhang M-Q (1989) The intestine as a model for neuronal plasticity. Arch Histol Cytol 52:167–180
Keast JR, Furness JB, Costa M (1984) Origins of peptide and norepinephrine nerves in the mucosa of the guinea pig small intestine. Gastroenterology 86:637–644
Kelly JP (1985) Reactions of neurons to injury. In: Kandel ER, Schwartz JH (eds) Principles of neural science, 2nd edn. Elsevier, New York Amsterdam Oxford, pp 187–195
Kobayashi S, Nishisaka T (1985) Myenteric enkephalin neurons around the laser-photocoagulation necrosis: an immunocytochemical investigation in the guinea pig jejunum and proximal colon. Arch Histol Jpn 48:239–254
Kobayashi S, Suzuki M, Nishisaka T (1989) Immunohistochemical studies on the regenerative features of nerve plexuses severed by spot irradiation with argon laser beam in the guinea-pig small intestine. Biomedical Res 10 [Suppl 3]:467–489
LeDouarin N, Teillet M-A (1973) The migration of neural crest cells to the wall of the digestive tract in avian embryo. J Embryol Exp Morphol 30:31–48
Mori N, Yoshizuka M, Ueda H, Ono E, Umezu Y, Fujimono S (1989) Ultrastructural findings in the wound healing of the colonic mucosa of rabbits. Acta Anat 134:82–88
Okada A, Okamoto E (1971) Myenteric plexus in hypertrophied intestine. J Neuro-Visceral Relations 32:75–89
Okamoto E, Ueda T (1967) Embryogenesis of intramural ganglia of the gut and its relation to Hirschsprung's disease. J Pediatr Surg 2:437–443
Papasova M, Atanassova E (1989) Adaptation to surgical perturbations. In: Schult SG, Wood JD, Rauner BB (eds) Handbook of physiology, section 6, vol I. Oxford University Press, Bethesda, Maryland, pp 1199–1224
Saffrey MJ, Burnstock G (1988) Peptide-containing neurons in explant cultures of guinea-pig myenteric plexus during development in vitro: gross morphology and growth patterns. Cell Tissue Res 254:167–176
Sarna S, Condon RE, Cowles V (1983) Enteric mechanisms of initiation of migrating myoelectric complexes in dogs. Gastroenterology 84:814–822
Trudrung P, Waldner H, Sklarek J, Nitsch C (1990) Lesion patterns of vasoactive intestinal polypeptide-containing neurons in the myenteric plexus induced by clamping or transection of rat jejunum. Neurosci Lett 109:277–281
Young HM, Furness JB, Sewell P, Burcher EF, Kandiah CJ (1993) Total numbers of neurons in myenteric ganglia of the guinea-pig small intestine. Cell Tissue Res 272:197–200
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Tokui, K., Sakanaka, M. & Kimura, S. Progressive reorganization of the myenteric plexus during one year following reanastomosis of the ileum of the guinea pig. Cell Tissue Res 277, 259–272 (1994). https://doi.org/10.1007/BF00327773
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DOI: https://doi.org/10.1007/BF00327773