Advances in the management of Hirschsprung disease
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1 Original Articles Altered Distribution of Interstitial Cells of Cajal in Hirschsprung Disease Udo Rolle, D; Anna Piaseczna Piotrowska, D; Laszlo Nemeth, D; Prem Puri, S, FRCS Context. Constipation or recurrent intestinal dysmotility problems are common after definitive surgical treatment in Hirschsprung disease (HD). c-kit positive interstitial cells of Cajal (ICCs) play a key role in the motility function and development of the gastrointestinal tract. Interstitial cells of Cajal that carry the tyrosine kinase receptor (c-kit) develop as either myenteric ICCs or muscular ICCs under the influence of the kit ligand, which can be provided by neuronal and nonneuronal cells, for example, smooth muscle cells. Objective. To investigate the distribution of myenteric and muscular ICCs in different parts of the colon in HD. ethods. Resected bowel specimens from 8 patients with rectosigmoid HD were investigated using combined staining with c-kit enzyme and fluorescence immunohistochemistry and acetylcholinesterase and nicotinamide adenine dinucleotide phosphate (NADPH) histochemistry in whole-mount preparations and conventional frozen sections. Results. In the normal bowel, ICCs formed a dense network surrounding the myenteric plexus and at the innermost part of the circular muscle. yenteric ICCs were absent or sparse in the aganglionic bowel and sparse in the transitional zone. The expression of myenteric ICCs in the ganglionic bowel in HD was reduced compared to that in the normal bowel, and they formed only sparse networks. uscular ICCs were found in the aganglionic bowel, transitional zone, and normoganglionic bowel of HD in a reduced density compared to the normal bowel. Conclusion. This study demonstrates altered distribution of ICCs in the entire resected bowel of HD patients. This finding suggests that persistent dysmotility problems after pull-through operation in HD may be due to altered distribution and impaired function of ICCs. (Arch Pathol Lab ed. 2002;126:928 9) Advances in the management of Hirschsprung disease (HD) afford most patients with HD a satisfactory outcome after definitive corrective surgery. However, some patients continue to have persistent bowel dysfunction despite adequate resection of the aganglionic bowel segment. Postoperative bowel dysfunction includes enterocolitis, constipation, and incontinence. 1 Postoperative enterocolitis occurs in 6% to 20% of patients, and its incidence is unrelated to the timing or type of definitive surgery. Constipation and soiling have been reported in 11% to % of patients after pull-through operations. 4, It is not known why these postoperative persistent bowel problems occur. Some investigators have suggested an association between increased risk of complications and a particular type of pull-through operation. 7 Others have not observed any correlation between postoperative bowel symptoms and the type of definitive procedure. 7 Similarly, the length of the aganglionic segment has not been found to influence the clinical outcome. 7 Persistent bowel problems after pull-through operations have led to increasing realization that within the pulled-through segment, the Accepted for publication arch 19, From the Children s Research Centre, Our Lady s Hospital for Sick Children, Dublin, Ireland (Drs Rolle and Piotrowska, and r Puri); Department of Paediatric Surgery, University of Szeged, Szeged, Hungary (Dr Nemeth). Reprints: Prem Puri, S, FRCS, FRCS(Ed), Children s Research Centre, Our Lady s Hospital for Sick Children, Crumlin, Dublin 12, Ireland ( ppuri@crumlin.ucd.ie). presence of normal ganglion cells is not sufficient as an indicator of satisfactory outcome. 6,7 The normal motility of the gastrointestinal tract depends on the enteric nervous system, the smooth muscle layers, and the interstitial cells of Cajal (ICCs). Interstitial cells of Cajal are pacemaker cells, which generate slow waves and facilitate active propagation of electrical events and neurotransmission in the bowel wall. 8 Interstitial cells of Cajal can be recognized either by their unique ultrastructure on electron microscopy or with the immunohistochemical demonstration of their surface receptor tyrosine kinase Kit (c-kit). Recent studies demonstrated that the c-kit receptor is essential for the development of the ICCs. esenchymal ICC precursors that carry the c-kit receptor require the kit ligand, which can be provided by neuronal cells or smooth muscle cells. According to the influence of the kit ligand from either neuronal or smooth muscle cells, the ICCs develop as either myenteric ICCs (ICC my s) or muscular ICCs (ICC mus s). 9 Gut innervation has a complex, -dimensional structure, which is difficult to appreciate on thin sections. The whole-mount preparation technique produces a -dimensional picture to better demonstrate the structure of neuronal networks and their relationship of branching and interconnecting nerve fibers to each other and to the neighboring tissues. This technique is therefore especially useful for the investigation of pathologic changes in the submucosal and myenteric plexuses and the neighboring tissues, such as hyperplasia of the plexuses or giant gan- 928 Arch Pathol Lab ed Vol 126, August 2002 Interstitial Cells of Cajal in Hirschsprung Disease Rolle et al
2 Table 1. Patient No. Age Sex Type of HD wk 7wk 2mo 4mo 4mo 11 mo 1 mo 20 mo F F Hirschsprung Disease (HD) Patients Aganglionic Segment, cm Transitional Segment, cm Ganglionic Zone, cm Outcome Chronic constipation Soiling glia. The main advantages for the histologic evaluation become obvious when whole-mount preparations are compared with sections. Sections only partially reveal the morphology of the nerve and glial cells, being dependent upon orientation and localization. On the other hand, whole-mount preparation reveals the morphology of the plexuses in full, making possible changes easy to see. The aim of this study was to examine the distribution of myenteric and muscular ICCs in all parts of the resected bowel specimen in rectosigmoid HD using a wholemount preparation technique. ATERIALS AND ETHODS Large bowel full-thickness specimens were obtained from 8 patients with classic rectosigmoid HD during pull-through operation. The patients ages ranged from 4 weeks to 20 months (Table 1). Normal large bowel (sigmoid colon) specimens were collected as control specimens from 4 children (age range 4 years to 12 years, boys and 1 girl) during bladder augmentation operation. The specimens were fixed in Zamboni solution for more than 24 hours and rinsed in phosphate-buffered saline. Parts of the specimen were rinsed in phosphate-buffered saline with 10% sucrose at 4 C overnight and subsequently frozen in n-octenyl succinic anhydride compound in liquid nitrogen. A whole-mount preparation was made of each specimen using fine-pointed forceps, microsurgical scissors, and a dissecting microscope. Initially the submucosa-mucosa layer was removed, followed by separation of longitudinal and circular muscle layers. The separated layers were fixed without stretching with finepointed pins on a Sylgard silicone elastomer tray (Dow Corning Europe, La Hulpe, Belgium). Acetylcholinesterase (AChE) and nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase histochemistry was used to confirm the diagnosis of HD. The n-octenyl succinic anhydride compound embedded specimens were cut into 8- m serial cryostat sections and stained with hematoxylin-eosin, AChE, and NADPH-diaphorase. For standard AChE histochemistry, frozen sections and whole-mount preparations were incubated at 7 C following the modification of Hanker et al of the method of Karnovsky and Roots For histochemical staining with NADPH-diaphorase, specimens were incubated in 1 mg/ml NADPH (Sigma, Dorset, United Kingdom), 0.1 mg/ml nitroblue tetrazolium (Sigma), and 0.% Triton-X in 0.0 mol/l Tris-HCl buffer (ph 7.6) at 7 C. Single enzyme and fluorescence immunohistochemistry were carried out with whole-mount preparations and frozen sections using 2 c-kit antisera (mouse monoclonal antibody, NCL-c-kit, 7AD8, Novocastra Laboratories, Newcastle upon Tyne, United Kingdom, dilution 1:100 in triethanolamine-buffered saline bovine serum albumin %/Triton 0.1% and rabbit polyclonal antibody, catalog No. sc-186, Santa Cruz Biotechnology, Santa Cruz, Calif, dilution 1:100 in triethanolamine-buffered saline bovine serum albumin %/Triton 0.1%). Nonspecific labeling was checked by omitting the respective primary antibody. The enzyme immunohistochemistry was conducted using the Streptavidin Alkaline Phosphatase Universal Kit (Immunotech, Inc, arseille, France). The alkaline phosphatase activity was visualized with fast red (Immunotech), yielding a red reaction product. The fluorescence immunohistochemistry was conducted with Texas red labeled secondary goat anti-rabbit and goat anti-mouse antibodies (olecular Probes, Leiden, The Netherlands, dilution 1:0 in phosphate-buffered saline). Double-staining was performed as combined c-kit enzyme immunohistochemistry with histochemistry for NADPH-diaphorase and AChE using whole-mount preparations and frozen sections. The staining results were evaluated using bright-field and confocal scanning laser microscopy (BIO-RAD 2000, Hamil Hamstead, United Kingdom). RESULTS Normal Sigmoid Colon Hematoxylin-eosin staining, AChE histochemistry, and NADPH-diaphorase histochemistry demonstrated normal submucous and myenteric plexus and normal intramuscular innervation. yenteric ICCs were found in wholemount preparations and frozen sections, forming a dense network surrounding the myenteric plexus (Figures 1, A and 2, A). These cells appeared as cells with large cell bodies and numerous processes connecting with each other and with nerve and muscle cells. The ICC mus swere found in abundance between the smooth muscle fibers and particularly at the innermost part of the circular muscle (Table 2), where they formed a dense network. The ICC mus s were small, long, bipolar cells with only 2 long processes and several short processes (Figure ). Aganglionic Bowel of HD Patients Acetylcholinesterase and NADPH-diaphorase histochemistry revealed typical features of the aganglionic bowel in all HD patients. Whole-mount preparations and conventional frozen sections showed absence of ganglia in the submucosal and myenteric plexus, presence of hypertrophic nerve fibers in the submucosal layer and in the space between the circular and longitudinal muscle, and increased AChE activity in the lamina propria mucosae. Whole-mount preparations and frozen sections displayed sparse and only single ICC my s at the level of the myenteric plexus between the circular and longitudinal muscle layers. These cells appeared mainly as thin and bipolar cells closely related to the hypertrophic nerve trunks (Figures 1, B and 2, B). uscular ICCs were markedly reduced in number compared to the number seen in normal bowel and were mainly expressed at the innermost layer of the circular muscle layer. Arch Pathol Lab ed Vol 126, August 2002 Interstitial Cells of Cajal in Hirschsprung Disease Rolle et al 929
3 90 Arch Pathol Lab ed Vol 126, August 2002 Interstitial Cells of Cajal in Hirschsprung Disease Rolle et al
4 yenteric ICCs uscular ICCs Table 2. Normal Sigmoid Colon Staining Pattern of Interstitial Cells of Cajal (ICCs)* Aganglionic Zone in HD / Transitional Zone in HD * HD indicates Hirschsprung disease;, no ICCs,, few ICCs;, moderate number of ICCs; and, many ICCs. Ganglionic Zone in HD Transitional Zone of the Bowel in HD Patients Whole-mount preparations and conventional sections of the transitional zone showed sparse and small ganglia in the myenteric and submucosal plexus, accompanied by hypertrophic nerve fibers at the same level. The AChE activity in the lamina propria was increased. yenteric ICCs were evident as single cells or cell clusters closely related to the small myenteric ganglia (Figure 2, C). The ICC my s did not form the typical networks seen in the normal bowel. uscular ICCs were found between the smooth muscle fibers and were mainly expressed at the innermost layer of the circular muscle layer. Their number was reduced compared to that in the normal bowel. Ganglionic Bowel in HD Patients Whole-mount preparations and conventional sections displayed normal-sized myenteric and submucosal plexuses in the specimens. Both plexuses showed normal numbers of ganglion cells and no evidence of hypertrophic nerve trunks. The AChE activity in the lamina propria was normal in 6 patients and still moderately increased in the remaining 2 patients. yenteric ICCs were found, but their number was still reduced compared to that observed in the normal bowel. The evident ICC my s formed sparse networks around the ganglia of the myenteric plexus in contrast to the dense ICC my s networks seen in normal bowel (Figure 2, D). The expression of the ICC mus s was normal in the smooth muscle layers, particularly at the innermost part of the circular muscle layer. COENT The role of ICCs as coordinators for intestinal motility has become apparent in the last few years. In the human bowel wall, the ICCs are localized at the level of the myenteric plexus between the longitudinal and circular muscle layers, in the deep muscular plexus in the innermost part of the circular muscle layer, and within the circular muscle layer itself. Previous studies have suggested major functions of ICCs: (1) they are pacemaker cells in smooth muscle, (2) they facilitate active propagation of electrical events, and () they mediate neurotransmission Recently it has been suggested that ICCs may produce nitric oxide and amplify inhibitory neurotransmission Loss of specific ICCs in the murine stomach resulted in the loss of nitric oxide dependent neurotransmission. 14,22 It is currently accepted that the cellular network of ICCs is connected by gap junctions to each other and to the muscle cells. 2 Gap junctions are transmembrane channels that allow the exchange of ions, metabolites, and other small molecules (less than dalton), including second messengers, such as cap, inositol triphosphate, and Ca 2, between the cytoplasm of adjacent cells. 24 Recent studies investigated the fetal and postnatal differentiation and development of ICCs in the human gastrointestinal tract. 2,26 c-kit positive ICCs were present in the stomach from 9. weeks gestation and in the small and large bowel from 12 to 1 weeks gestation. The distribution of the ICCs varies with gestational age and region in the gastrointestinal tract, and maturation of ICCs continues postnatally. 2,26 With increasing age, dense networks of ICCs are found around the myenteric plexus, and numerous ICC mus s are expressed within the muscle layers and particularly at the innermost part of the circular muscle. Furthermore, the myenteric ICCs showed an increased cell size and increased number of individual cytoplasmic processes during early development. Lack of ICCs causes gastrointestinal motility disorders or symptoms of pseudo-obstruction in animal models. 27,28 W/W V mutant mice have deficient ICCs in the small intestine myenteric plexus, which leads to absent electrical slow waves and abnormal, slow, and uncoordinated motility. 29 Absence of electrical slow waves leads to decreased and irregular smooth muscle contractility in the gut and results in impaired intestinal transit. Blockade of the ICCs by an antagonistic anti-c-kit antibody resulted in a severe motility dysfunction in mice. 0 The crucial role of the tyrosine kinase receptor c-kit at the surface of the mesenchymal ICC precursors has been shown in various previous studies. Under the influence of the kit ligand or stem cell factor provided by neuronal cells of the myenteric plexus, a group of ICC precursors develops to myenteric ICCs with greater amounts of cytoplasm and multiple processes. In mice with mutations of the kit Figure 1. A, Dense network of c-kit positive myenteric interstitial cells of Cajal (ICC my s) around the myenteric plexus in normal colon. B, Single c-kit positive ICC my s around hypertrophic nerve trunks in the aganglionic bowel in Hirschsprung disease (streptavidin alkaline phosphatase method, NADPH-diaphorase histochemistry, original magnification 200). Figure 2. A, Dense network of c-kit positive myenteric interstitial cells of Cajal (ICC my s) around the myenteric plexus in normal colon (original magnification 200). B, Single, thin ICC my s around hypertrophic nerve trunks in the aganglionic bowel in Hirschsprung disease (HD) (original magnification 400). C, Single ICC my s around defective myenteric plexus in the transitional zone in HD. Note small myenteric ganglia (original magnification 400). D, Group of ICC my s around the myenteric plexus in the ganglionic bowel in HD (whole-mount preparation, streptavidin alkaline phosphatase method, NADPH-diaphorase histochemistry, original magnification 00). Figure. Normal muscular interstitial cells of Cajal within the intestinal smooth muscle layer (whole-mount preparation, streptavidin alkaline phosphatase method, NADPH-diaphorase histochemistry, original magnification 00). Arch Pathol Lab ed Vol 126, August 2002 Interstitial Cells of Cajal in Hirschsprung Disease Rolle et al 91
5 ligand, abnormal network of myenteric ICCs was found. 1 Another group of ICC precursors is believed to be influenced by the kit ligand provided by smooth muscle cells, consequently leading to the development of ICC mus s that usually appear as smaller bipolar cells. These studies suggest that at least a certain group of ICCs does not require intact enteric neurons for their development or maintenance. 1 Altered distributions of ICCs have been described in several disorders of human intestinal motility, including hypertrophic pyloric stenosis, 4 HD, 7 intestinal pseudoobstruction, 8 40 slow-transit constipation, 41 and ulcerative colitis. 42 Vanderwinden et al described scarce ICCs with disrupted network in the aganglionic bowel, whereas the distribution of ICCs in the ganglionic bowel of HD was similar to that observed in the controls. These ICCs did not form a network and showed no clear relation to the hypertrophic nerve trunks. Yamataka et al 6,7 found few c-kit positive cells in the muscle layers in HD and a moderate number around the thick nerve bundles in the space between the 2 muscle layers in the aganglionic bowel. Horisawa et al 4 reported no differences in c-kit immunopositive cells in aganglionic segments compared with the corresponding area of ganglionic bowel. The study referred to the importance of regional differences in the distribution of c-kit positive cells in the normal colon, but not to the different types of ICCs, such as myenteric and muscular ICCs. Previous studies did not examine the reported expression of ICCs in the transitional zone. The present study showed that ICC my s and ICC mus s are expressed differently in rectosigmoid HD compared to normal bowel. yenteric ICCs were found to be markedly reduced not only in the aganglionic bowel, but also in the transitional zone and ganglionic part of HD bowel. In contrast, ICC mus s were markedly reduced in the aganglionic bowel, moderately reduced in the transitional zone, and were present in normal numbers in the ganglionic bowel in HD. Reduction of ICC my s in the normoganglionic sigmoid colon in HD may be the cause for the dysmotility disturbances seen in many patients after pull-through operation due to the defective transmission of electrical events between the enteric nervous system and adjacent smooth muscle. Due to the developmental relationship between the enteric nervous system and the ICC my s, the defective expression of ICC my s in rectosigmoid HD may be of primary origin. However, the data in the present study do not exclude the possibility that the observed defects in ICCs may be secondary to other factors, such as neuropathies or chronic constipation. The relationship between the ICCs and the enteric nervous system is complex, and its investigation using only section preparations is not sufficient. The whole-mount preparation technique provides better assessment of the - dimensional topography of the ICC networks around the myenteric plexus and within the muscle layers of the bowel. This method has been used in previous studies of the normal and defective expression of ICCs. Horisawa et al 4 described the -dimensional configuration of c-kit positive cells as typical multipolar cells around the myenteric plexus and slender bipolar cells within the circular and longitudinal muscle layers. A recent study revealed clear colocalization of ICCs and nitrergic innervation in wholemount preparations of the normal gut. 44 A meshlike network of NADPH-diaphorase positive nerve fibers in the myenteric plexus was surrounded by a reticular network of c-kit positive ICCs. In another study, whole-mount preparations of guinea pig small intestine revealed closed relationships between ICC mus s and nitric oxide synthase, vesicular acetylcholine transporter, and substance P like immunoreactivities. 4 Hence, the enteric motoneurons, ICCs, and smooth muscle cells form functional units that release transmitter and mediate and transduce neural inputs into mechanical responses in the gut. The deficient expression of ICCs in the aganglionic bowel may contribute to motility dysfunction in HD by defective generation of electrical pacemaker activity. 46 This study was supported by grant RO 2291/1-1 from Deutsche Forschungsgemeinschaft, Bonn, Germany (Dr Rolle). References 1. So HB, Becker J, Schwartz DL. Eighteen years experience with neonatal Hirschsprung s disease treated by endorectal pull-through without colostomy. J Pediatr Surg. 1998;: Quinn FJ, Fitzgerald RJ, Guiney EJ, O Donnell B, Puri P. Hirschsprung s disease. In: Hadziselimovic F, Herzog B, eds. 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