Nervous system development in normal and atresic chick embryo intestine: an immunohistochemical study

Abstract

Intestinal motility disorders are a common complication after surgery for neonatal intestinal atresia. Although intestinal atresia causes alterations in the enteric nervous system, especially in its inner structures (nervous fibers in the mucosa, submucous and deep muscular plexuses), how these alterations develop is unclear. The chick model is a useful research tool for investigating the ontogenesis of the enteric nervous system and the pathogenesis of congenital bowel diseases. More information is needed on the overlap between the developing enteric nervous system and intestinal atresia. Because vasoactive intestinal polypeptide and substance P are typical intestinal neuropeptides, and vasoactive intestinal polypeptide acts as a modulator in neurodevelopment and an inhibitor of smooth muscle cell proliferation, our aim in this study was to investigate the distribution of their immunoreactivity in the developing enteric nervous system of normal and experimental chick models. We studied gut specimens excised from normal chick embryos (aged 12-20 days) and experimental chick embryos (aged 15-20 days) that underwent surgical intervention on day 12 to induce intestinal atresia (atresic embryos) or simply to grasp the bowel loop (sham-operated embryos). In normal chick embryos we showed vasoactive intestinal polypeptide and substance P immunoreactivity from day 12 in the submucous and myenteric plexuses. The distribution of peptide immunoreactivity differed markedly in atresic and normal or sham-operated gut embryos. These differences especially affected the inner structures of the enteric nervous system of specimens proximal to atresia and were related to the severity of dilation. Because nerve structures in the gut wall mucosa and submucous and deep muscular plexuses play a role in motility control and stretch sensation in the intestinal wall, our findings in the chick embryo may help to explain how gut motility disorders develop after surgery for neonatal intestinal atresia.

Endocrine cells in atresic chick embryo intestine: histochemical and immunohistochemical study

“…On the other hand, previous studies using neuronal markers point the asynchronic development of the myenteric plexus, which appears delayed below the obstacle and accelerated above in human intestinal atresic specimens (Khen et al , 2004). The increase of endocrine cell population in severely dilated proximal bowel correlates with a disorganization and reduction of peptidegic nerve network that we found at a later embryonic age (Parisi Salvi et al , 2004). A close relation between endocrine cells and nerve network in abnormal functioning bowel was already shown in the colon of patients with Hirschsprung’s disease where the number of endocrine cells in the aganglionic segment was significantly increased, compared with the ganglionic segment (Soeda et al , 1993).…”

“…This increase depended on the precociousness of the surgery and the severity of the dilation of proximal bowel. However, previous works showed the relation between the degree of dilation and the severity of changes in the enteric nervous system (Masumoto et al , 1999; Parisi Salvi et al , 2004). …”

“…Although intestinal atresia causes alterations in the enteric nervous system, especially in its inner structures as nervous fibers in the mucosa, submucous and deep muscular plexuses (Masumoto et al , 1999; Schoemberg and Kluth, 2002; Parisi Salvi et al , 2004; Fiegel et al , 2006), the physiopathology of the motility disorders remains unknown. It is a complex process because of the multiplicity of factors implicated in the genesis of the peristaltic reflex and the overlap between the developing enteric neuroendocrine system and intestinal atresia.…”

“…We used an experimental chick model (Baglaj et al , 2001) that reproduces the most common type of intestinal atresia found in newborn babies (type II intestinal atresia) (Grosfeld et al , 1979) by transforming a jejunoileal segment into a fibrotic cord that separates two blind ends proximal and distal to the atresic stump. In this model we have just investigated the development of the enteric nervous system (Parisi Salvi et al , 2004). Our aim was to investigate the distribution of enteroendocrine cell population with particular regards to serotonin and neurotensin immunoreactive cells in atresic embryos.…”

Endocrine cells in atresic chick embryo intestine: histochemical and immunohistochemical study

“…ntestinal motility disorders are a common complication after surgery for neonatal intestinal atresia. Although intestinal atresia causes alterations in the enteric nervous system, especially in its inner structures as nervous fibers in the mucosa, submucous and deep muscular plexuses (Masumoto et al, 1999;Schoemberg and Kluth, 2002;Parisi Salvi et al, 2004;Fiegel et al, 2006), the physiopathology of the motility disorders remains unknown. It is a complex process because of the multiplicity of factors implicated in the genesis of the peristaltic reflex and the overlap between the developing enteric neuroendocrine system and intestinal atresia.…”