Abstract
Knowledge regarding the foetal and postnatal development of the enteric nervous system is crucial for the understanding of congenital disorders. While lot of information exists regarding the myenteric and submucosal plexuses, the development of the mucosal plexus has not been previously studied. The mucosal innervation seems to play an important role in the local reflex activity of the gut. In this study, we examined the development of enteric mucosal innervation in the pig at various ages of life. Small and large bowel paraffin-embedded specimens were stained with PGP 9.5 and neurofilament protein in three piglets from six age groups (60 and 90 days gestation, newborn, 4 and 12 weeks old, and adult pigs). Small and large bowel demonstrated identical innervation patterns. Myenteric and submucosal plexuses were stained with PGP 9.5 at 60 days gestation. However, the mucosal staining was first noted clearly at the newborn period. By 4 weeks, PGP 9.5 staining was noted in small amounts within the mucosa. Inner proprial and villous fibres were seen ahead in time to the subepithelial fibres. Both inner proprial and villous staining became quiet prominent by 12 weeks of age and remained unchanged into adulthood. However, the subepithelial fibres appear to increase in adulthood. This study demonstrates for the first time that enteric mucosal innervation first appears only at birth. The immaturity of the mucosa generated reflex activity, and secretory functions may have implication in the management of functional intestinal obstruction in the premature infant.
Similar content being viewed by others
References
Bayliss WM, Starling EH (1899) The movements and innervation of the small intestine. J Physiol 24:99–143
Mall F (1896) A study of the intestinal contraction. Johns Hopkins Hosp Rep 1:37–75
Stohr P (1934) Mikroskopische studien zur Innervation des Magendarmkanals III. Z ZellForsch 21:243–278
Stohr P (1949) Mikroskopische Studien zur Innervation des Magendarmkanales V. Z ZellForsch 34:1–37
Lassmann G (1975) Finding of ganglion cells in the mucosa of the colon, sigmoid flexure, and rectum (author’s transl). Virchows Arch A Pathol Anat Histol 365:257–261
Timmermans JP, Scheuermann DW, Stach W, Adriaensen D, De Groodt-Lasseel MH (1990) Distinct distribution of CGRP-, enkephalin-, galanin-, neuromedin U-, neuropeptide Y-, somatostatin-, substance P-, VIP- and serotonin-containing neurons in the two submucosal ganglionic neural networks of the porcine small intestine. Cell Tissue Res 260:367–379
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
Balemba OB, Hay-Schmidt A, Assey RJ, Kahwa CK, Semuguruka WD, Dantzer V (2002) An immunohistochemical study of the organization of ganglia and nerve fibres in the mucosa of the porcine intestine. Anat Histol Embryol 31:237–246
Mestres P, Diener M, Rummel W (1992) Electron microscopy of the mucosal plexus of the rat colon. Acta Anat (Basel) 143:275–282
Mestres P, Diener M, Rummel W (1992) Histo- and immunocytochemical characterization of the neurons of the mucosal plexus in the rat colon. Acta Anat (Basel) 143:268–274
Kunze WA, Bornstein JC, Furness JB (1995) Identification of sensory nerve cells in a peripheral organ (the intestine) of a mammal. Neuroscience 66:1–4
Sabate JM, Coffin B, Jian R, Le Bars D, Bouhassira D (2000) Rectal sensitivity assessed by a reflexologic technique: further evidence for two types of mechanoreceptors. Am J Physiol Gastrointest Liver Physiol 279:G692–G699
Wedel T, Roblick U, Gleiss J, Ott V, Eggers R, Kuhnel W, Krammer HJ (1999) Disorders of intestinal innervation as a possible cause for chronic constipation. Zentralbl Chir 124:796–803
Hens J, Vanderwinden JM, De Laet MH, Scheuermann DW, Timmermans JP (2001) Morphological and neurochemical identification of enteric neurones with mucosal projections in the human small intestine. J Neurochem 76:464–471
Cornelissen W, Timmermans JP, Van Bogaert PP, Scheuermann DW (1996) Electrophysiology of porcine myenteric neurons revealed after vital staining of their cell bodies. A preliminary report. Neurogastroenterol Motil 8:101–109
Timmermans JP, Scheuermann DW, Stach W, Adriaensen D, De Groodt-Lasseel MH (1992) Functional morphology of the enteric nervous system with special reference to large mammals. Eur J Morphol 30:113–122
Timmermans JP, Adriaensen D, Cornelissen W, Scheuermann DW (1997) Structural organization and neuropeptide distribution in the mammalian enteric nervous system, with special attention to those components involved in mucosal reflexes. Comp Biochem Physiol A Physiol 118:331–340
Kararli TT (1995) Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm Drug Dispos 16:351–380
de Lorijn F, Voskuijl WP, Omari TI, Kok JH, Taminiau JA, Benninga MA (2005) Assessment of the rectoanal inhibitory reflex in preterm infants with delayed meconium passage. J Pediatr Gastroenterol Nutr 40:434–437
de Lorijn F, Omari TI, Kok JH, Taminiau JA, Benninga MA (2003) Maturation of the rectoanal inhibitory reflex in very premature infants. J Pediatr 143:630–633
Kubota M, Suita S, Kamimura T (1997) Abnormalities in visceral evoked potentials from the anal canal in children with chronic constipation. Surg Today 27:632–637
Kubota M, Nagasaki A, Sumitomo K (1992) Manometric evaluation of children with chronic constipation using a suction-stimulating electrode. Eur J Pediatr Surg 2:287–290
Kamm MA, Lennard-Jones JE (1990) Rectal mucosal electrosensory testing—evidence for a rectal sensory neuropathy in idiopathic constipation. Dis Colon Rectum 33:419–423
Deen KI, Premaratna R, Fonseka MM, De Silva HJ (1998) The recto-anal inhibitory reflex: abnormal response in diabetics suggests an intrinsic neuroenteropathy. J Gastroenterol Hepatol 13:1107–1110
Vanner S, Macnaughton WK (2004) Submucosal secretomotor and vasodilator reflexes. Neurogastroenterol Motil 16(Suppl. 1):39–43
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Paran, T.S., Rolle, U. & Puri, P. Postnatal development of the mucosal plexus in the porcine small and large intestine. Pediatr Surg Int 22, 997–1001 (2006). https://doi.org/10.1007/s00383-006-1786-5
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00383-006-1786-5