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Prenatal Development of the Myenteric Plexus in Human Sigmoid Colon

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Prenatal Development of the Myenteric Plexus in Human Sigmoid Colon Original article Prenatal development of the myenteric plexus in human sigmoid colon Singh, S.1*, Shariff, A.1, Roy, T.S.1 and Kumar, H.2 1Department of Anatomy, All India Institute of Medical Sciences, New Delhi, 110029, India 2Department of Neurosurgery, All India Institute of Medical Sciences, New Delhi, 110029, India *E-mail: [email protected] Abstract Introduction: The enteric nervous system rivals the brain in complexity and can function independently. There are numerous reports on its development in gut but the literature is scant on the development of myenteric plexus in human sigmoid colon which is a site of various congenital and acquired diseases. This study represents a detailed qualitative morphometric analysis of the development of human sigmoid colonic innervation during second trimester. Material and Methods: Sigmoid colon from 12 aborted foetuses aged 14-23 weeks of gestation were processed for cresyl violet staining and NADPH-d histochemistry. Results: At 14weeks of gestation, both myenteric plexus and submucosal plexus were present and the size of the neurons with thickness of circular muscle was increased from 14-23weeks. Between 14-23weeks, there was remarkable increase in neuropil and nerve fibres in circular muscle. The neurons were more numerous in the mesenteric zone. Conclusion: There is an increase in the neuron size from 14-23weeks signifying maturational process. The circular muscle plexus is well developed at 23weeks. This study also revealed that there is correlation between the development of the circular muscle layer and the myenteric plexus. This study supports previous suggestions that nitrergic neurons are the subpopulation of neurons present in myenteric plexus. Such studies may answer important questions regarding the normal and pathologic development of the enteric nervous system. Keywords: enteric nervous system, myenteric plexus, sigmoid colon, weeks of gestation, submucosal plexus. 1 Introduction The gastrointestinal tract in vertebrates is an unique in various species, the investigation of human development biological structure that has an independent nervous system is necessary in order to establish the basic rules of the which rivals the brain in complexity, known as the enteric development of the human ENS. At the same time, clinical nervous system (ENS). The ENS has been described as a studies revealed that congenital malformations of the ENS “second brain” (GERSHON, 1998). The second brain seriously affect the gut motility, gastric acid secretion, and contains some 100 million neurons, more than in either the water and electrolyte transport (UEDA and OKAMOTO, spinal cord or the peripheral nervous system. These neurons 1967). Since the innervation of the human gut is relatively helps in breaking down food, absorbing nutrients, and mature at birth, the study of the development of the ENS expelling of waste require chemical processing, mechanical requires the use of foetal gut tissue (ERDE and GERSHON, mixing and rhythmic muscle contractions that move the 1981; FURNESS and COSTA, 1987). The development contents in the gut. Gershon says that feeling of butterflies and maturation of the ENS in the sigmoid colon in humans in the stomach signifies signaling in the gut as part of our has not been studied. The maturation of myenteric plexus physiological stress response (WADE, GERSHON and (MP) peaks in second trimester especially from 16-20weeks KIRCHGESSNER, 1994). Despite of high degree of of gestation (WG) in esophagus (HITCHCOCK, PEMBLE, complexity and its similarities to the CNS, the ENS is derived BISHOP et al., 1992), the present study was designed to from the neural crest cells (NCC) which is the source of all evaluate the morphological maturation of the human branches of peripheral nervous system (LE DOUARIN, sigmoid colon during similar time period. 1982). The sigmoid colon (SC) is a site of various congenital and 2 Materials and Methods acquired diseases. The developing enteric nervous system (ENS) has a role in colonic diseases. Some researchers are 12 fresh foetuses were used for the present study from the focused on a particular disorder such as Hirschsprung’s foetal repository in the department of anatomy (collected disease, while others are doing research on general principles at different times from the labour room of Department of regarding structure and function. It has been seen that Obstetrics and Gynaecology, All India Institute of Medical the results on small laboratory animals cannot simply be Sciences, New Delhi). All the foetuses used in the study extrapolated to humans (BURNSTOCK and HOYLE, were collected in accordance with the protocol approved 1989; ERDE and GERSHON, 1981; COSTA, BROOKES by the Ethics Committee, All India Institute of Medical and STEELE, 1991). Since the morphological and Sciences, New Delhi. The foetuses less than 20 WG neurochemical properties of the enteric plexuses are different were obtained from cases where medical termination of 156 J. Morphol. Sci., 2013, vol. 30, no. 3, p. 156-166 Prenatal development of the myenteric plexus in human sigmoid colon pregnancy was performed for family planning (legalized in intense (45min-60 min) by washing the tissues gently India under MTP Act, 1971) while those more than 20WG with chilled 0.1 M phosphate buffer and the sections were were stillbirths. None of the mothers suffered from any mounted in a mixture of glycerol and phosphate buffer medical illness during pregnancy and the foetuses used in (4:1) for morphological studies (KIMURA, SINGLE and the study had no congenital anomalies. However, the causes VINCENT, 1983). The stained sections were examined of death of the stillbirths were undetermined. Immediately under a microscope and images were captured using a after arrival in the laboratory, the foetuses were weighed CCD (charge-coupled-device) camera connected to a frame and measured for crown rump length, foot length and grabber card in an IBM PC interfaced with a Zeiss binocular biparietal diameter (LACERDA, 1990; SAILAJA, AHUJA microscope. The images were saved as JPEG with minimum and GOPINATH, 1996). Together with above parameters compression and maximum quality. and the clinical history, the foetal age was determined. After making a paramedian incision in the abdomen the foetuses were immersed in 4% buffered paraformaldehyde 3 Results for proper fixation. Most of the specimens used in the present study were obtained within 6-8 hours after delivery 3.1 Cresyl violet stained sections and were preserved at 4 °C to minimize the post-mortem Under low magnication, mesentery was noted attached changes. Sigmoid colon was identified by its mesentry and to the superficial surface of the colons of all foetuses studied. dissected out immediately. A portion of the sigmoid colon Colonic lumen and mucosal folds were clearly visible was removed and kept in the appropriate fixative for further (Figure1a-f). The colon was covered by thick serosa. Well evaluation. developed mesentery was present in the colon (Figure 2a). By The Cresyl violet staining of paraffin sections and 14 WG, the colonic wall thickness was more in comparison NADPH diaphorase histochemistry - enzyme histochemistry to the lumen size (Figure 1a). By 14 WG, both the MP techniques were used to study the tissue preparations. For and SP were developed in the sigmoid colon (Figure 3A). Cresyl violet staining, after proper fixation in 4% buffered The myenteric ganglia(MG) was present between inner paraformaldehyde for 7 days, the colon tissue were circular muscle(CM) and outer longitudinal muscle(LM) dissected to make small tissue blocks. The blocks were layer (Figure 2A, a). The submucosal plexus(SP) was washed with phosphate buffer for 5-6 times for removing characterised by scattered neurons in the submucosa of the the extra fixative. The tissue was then processed for paraffin colon (Figure 3A). The MG of the MP was spheroidal and embedding. The tissue was sectioned at 7µ thickness using elongated in shape (Figure 3A). The various portions of the a rotary microtome [Microme (GmBh) microtome]. The MG were adjacent to each other and were interconnected sections were hydrated after passing through xylene and by fibers. At mesenteric border, the ganglia were usually descending grades of alcohol. The sections were stained in spheroidal and elongate in shape at antimesenteric border 0.1% cresyl violet in distilled water for 10 min at 37 °C. (Figure 2a). The capsular cells were deeply stained with cresyl The stained sections were rinsed in distilled water and violet and surrounded the ganglia (Figure 3B). Neuronal cells then differentiated in 96% alcohol until only the Nissl were small with round nuclei and occasionally contained two substance was stained purple. The differentiation process nucleoli representing immature neuroblasts (Figure 3 A, B). was controlled visualising under a microscope. The sections Little Nissl substance were present and the neuronal cells were dehydrated rapidly in absolute alcohol, cleared in had scanty cytoplasm (Figure 3B). Neuronal cells of xylene and mounted in DPX. different shapes were arranged in a compact manner in the For NADPH diaphorase histochemistery, colonic tissue ganglia especially on the outer surface of the CM and these was fixed in fresh 4% buffered paraformaldehyde for 2 hours cells were appearing larger than the other cells (Figure 2a). at 4 °C. They were washed thoroughly after fixation in chilled 0.1 M phosphate buffer and then cryoprotected in 15% and Neurons were more numerous at the mesenteric border than 30% sucrose at 4 °C for 3 hours and 8 hours (till tissue sinks) the free surface of the gut (Figure 2a). Smaller cell profiles of respectively. The samples were frozen in OCT (optimum immature glial cells were also noted (Figure 3A, B). Scattered cutting temperature) compound (Tissue Tek) and 20µ thick neurons were present in submucosa on the inner surface of sections were cut using a cryostat (Leica). Frozen sections CM. The submucosal neurons were of same size as of the were mounted onto 1% gelatin coated slides. Slides were myenteric plexus.
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