Case Report: Unusual Type of Colonic Neuromuscular Disorder with Extensive Vacuolization
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1 Available online at Annals of Clinical & Laboratory Science, vol. 38, no. 2, Case Report: Unusual Type of Colonic Neuromuscular Disorder with Extensive Vacuolization Sandhya Sundaram, 1 Robert E. Brown, 2 and Ping L. Zhang 3 1 Department of Pathology, Sri Ramachandra Medical College, Porur, Chennai, India, 2 Department of Pathology, University of Texas Health Sciences Center, Houston, Texas, and 3 Department of Anatomic Pathology, William Beaumont Hospital, Royal Oak, Michigan Abstract. Various pathological abnormalities of smooth muscle and innervation result in clinical syndromes with disordered motility of the small intestine and colon. Although these abnormalities have been extensively reported clinically, their pathologic changes and pathophysiologic mechanisms have not been well elucidated. We report a case of visceral neuropathy with secondary muscle changes in a 7-yr-old ventilator dependent, mentally retarded child who presented with a history of chronic constipation and symptoms of intestinal obstruction. The muscle layer of the colectomy specimen showed extensive infiltration of vacuolated cells that were positive for S-100 and synaptophysin but negative for glial fibrillary acidic protein (GFAP) and neural filament protein (NFP). Calretinin positivity was preserved in submucosal ganglion cells but was absent in vacuolated nerve branches. Masson s trichrome stain showed evidence of fibrosis, indicative of muscle damage. There was a reduced number of intestinal cells of Cajal in the muscularis propria, as indicated by CD117 (c-kit) immunostaining. This disorder is most likely a sporadic visceral neuropathy, secondarily affecting muscular function, that causes colonic pseudo-obstruction. Keywords: colon, neuromuscular disorder, calretinin, vacuolization Introduction Gastrointestinal motility is a function of gastrointestinal smooth muscle that is controlled by the intrinsic and extrinsic nerves of the gastrointestinal tract and, to a lesser degree, by gastrointestinal hormones. Theoretically, any abnormality of these factors can cause gastrointestinal dysmotility [1]. The clinical syndromes may include loss of normal peristalsis and transport, loss of sphincter tone or relaxation, occurrence of spontaneous uncoordinated contractions, and loss of normal cyclical events such as migrating motor complexes. These disorders may be functional with no recognizable Address correspondence to Ping L. Zhang, M.D., Ph.D., Department of Anatomic Pathology, William Beaumont Hospital, 3601 West 13 Mile Road, Royal Oak, MI 48073, USA; tel ; fax ; ping. zhang@beaumont.edu. morphologic abnormalities or they may be structural with defects evident on microscopy [2]. Most of these cases present with features of pseudoobstruction of the intestines, abdominal distension, or chronic constipation. Treatment is mainly symptomatic and supportive. Surgery may be helpful in selected cases that do not respond to medical measures. We report an unusual case of visceral neuropathy in a mentally retarded child who presented with intestinal obstruction. Clinical History A 7-yr-old ventilator-dependent, mentally retarded child presented with chronic constipation and symptoms of intestinal obstruction. Her medical history included an unknown metabolic disease, hypotonia, hypothermia, bradycardia, neurogenic bladder, seizure disorder, cortical blindness, chronic respiratory failure, and hypoglycemia She was /08/ $ by the Association of Clinical Scientists, Inc.
2 144 Annals of Clinical & Laboratory Science, vol. 38, no. 2, 2008 receiving continuous feeding of Pediasure with fiber and water. The patient had been in her usual clinical status until 9 days prior to admission when she began to develop abdominal distention, decreased bowel sounds, and decreased stool output. There was no blood or mucus in the stools. Two days later she began to have increased gastrictube residuals with bile retention of ml over 2 hr. She was afebrile throughout this period. She was suspected to have bowel obstruction and was transferred to the gastroenterology emergency department. On admission, her physical indices included pulse rate, 49/min; respirations, 12/min; blood pressure, 104/47 mm Hg; oxygen saturation, 100% at the ventilation setting and tidal volume of 320 ml. Her abdomen was distended and tympanic. No hepatosplenomegaly was noted. Laboratory investigations revealed metabolic acidosis and mild dehydration. Since she was found to have a dilated ascending colon, a hemicolectomy was performed. During the postoperative period, while she was receiving total parental nutrition, the patient developed severe hyperglycemia and was treated with iv insulin to normalize her blood glucose level. On the day of discharge from the hospital, she had adequate stool output and was tolerating her feedings. She had one episode of abdominal distension about 7 mo later, which resolved upon conservative treatment. Pathological Examination The operative specimen consisted of the right colon, about 28 cm in length, including a portion of cecum, 2 cm of ileum, and a 7 cm vermiform appendix. A moderate amount of pale mesenteric tissue was attached. The colon was dilated, averaging 6 cm diameter at the level of the ileocaecal valve and 4 cm diameter at the distal margin. The specimen was opened along the anti-mesenteric margin and it contained abundant brown liquid stool. The mucosa was pale pink with mild flattening of the normal architecture. There was no thickening, induration, or stricture of the colonic wall. The ostium to the appendix was patent. There was neither gross mucosal lesions nor congestion. Mesenteric tissue contained 18 lymph nodes. Many sections were taken for routine H&E staining. Selected sections were stained immunohistochemically for S-100, CD117, glial fibrillary acidic protein (GFAP), neural filament protein (NFP), calretinin, synaptophysin, inhibin-alpha, and CD68, using Dako antibodies and an autostainer (Dako Cyto-mation, Carpinteria, CA). Results Histological examination of the colonic mucosa was unremarkable. The muscularis mucosae and muscularis propria were thickened. The most remarkable finding was the presence of vacuolated cells with foamy cytoplasm diffusely scattered throughout the smooth muscle layer (Fig. 1A and 1B). The myenteric plexus showed ganglion cells and slightly vacuolated never fibers. The muscularis propria contained foci of degenerated muscle cells with replacement fibrosis. Trichrome staining confirmed the presence of fibrosis in the muscularis mucosae and muscularis propria (Fig. 1C). The vacuolated cells were negatively stained for CD68, inhibin-alpha, and PAS with diastase, ruling out histocytic infiltration and granular cell tumor. Immunohistochemistry showed that the vacuolated cells were strongly positive for S-100 (Fig. 1D). In addition, the vacuolated cells were weakly positive for synaptophysin. Submucosal ganglion cells were present with positive staining for calretinin, but were surrounded by vacuolated cells (Fig. 1E). In the myenteric plexus, ganglion cells were negative for calretinin staining, but nerve fibers were weakly positive for calretinin staining (Fig. 1F). The vacuolated cells showed entirely negative staining for calretinin (Fig. 1F). In the myenteric plexus, nerve fibers were stained weakly positive for both GFAP and NFP, but the vacuolated cells were stained negatively for both markers. The muscularis propria showed diminished interstitial cells of Cajal as indicated by lack of CD117 staining in cytoplasm. There were up to 5 interstitial cells of Cajal per mm 2 in muscularis propria when the nuclei of CD117-positive cells were counted. Colonic muscularis propria in two age-matched control cases showed approximately 15 interstitial cells of Cajal per mm 2. In view of the vacuolated S-100 positive cells, the reduced number of
3 Gastrointestinal neuromuscular disorder 145 Fig. 1. Visceral neuropathy with secondary muscular degeneration. Vacuolated cells with foamy cytoplasm are diffusely scattered throughout the muscularis propria (A: H&E stain, x40; B: H&E stain, x400). Fibrosis is present in muscularis propria (C: trichrome stain, x400). Vacuolated cells are positive for S-100 (D: S-100 stain, x400). Submucosal ganglion cells are positively stained for calretinin, but are surrounded by the vacuolated cells (E: calretinin stain, 600). Despite weakly positive staining in myenteric nerve fibers, the myenteric ganglion cells (arrow) and the vacuolated cells are negatively stained for calretinin (F: calretinin stain, x600).
4 146 Annals of Clinical & Laboratory Science, vol. 38, no. 2, 2008 interstitial cells of Cajal, and the presence of fibrosis in the muscle layer, a primary visceral neuropathy with secondary muscle changes was considered to be most likely as the cause of colonic pseudoobstruction. Discussion Table 1. Classification of visceral neuropathies, modified from Krishnamurthy and Schuffler [2}. A. Familial visceral neuropathies 1. Recessive, with intranuclear inclusions 2. Recessive, with mental retardation and calcification of the basal ganglia 3. Dominant, with neither of the above B. Sporadic visceral neuropathies. 1. Degenerative, non-inflammatory 2. Degenerative, inflammatory a. Paraneoplastic b. Non-paraneoplastic c. Isolated axonopathy C. Developmental abnormalities 1. Hirschsprung s disease 2. Total colonic aganglionosis 3. Maturational arrest a. With mental retardation b. With other neurologic abnormalities c. Isolated to myenteric plexus, without above 4. Neuronal intestinal dysplasia a. With neurofibromatosis b. With MEA II c. Isolated to intestine, without above D. Severe, idiopathic constipation E. Drug induced/toxic damage Intestinal pseudo-obstruction can result from either visceral neuropathy or visceral myopathy. In a study of 20 cases of chronic intestinal pseudoobstruction, a majority was visceral myopathy followed by neuropathy [3]. The most common symptoms include nausea, vomiting, abdominal distension, abdominal pain, and constipation or diarrhea [4]. Visceral neuropathies are commonly sporadic although there have been reports of familial cases [5]. In contrast, visceral myopathies tend to be familial. Most patients with visceral myopathy have light microscopic changes of smooth muscle fibrosis and vacuolar and other degenerative changes in the circular and longitudinal layers of the intestinal wall, although the changes often involve only one muscle layer [6]. Visceral neuropathies are characterized by degenerative changes in the myenteric plexus and loss of neurons and axons [7]. A classification of visceral neuropathy is listed in Table 1, based on a review by Krishnamurthy and Schuffler in 1987 [2]. Since cases of visceral neuropathy are seldom seen, no better classification has evolved during the past 20 years. Our patient had no family history of visceral neuropathy and her colonic lesion was not suggestive of one type of familial visceral neuropathy (Class A). Severe idiopathic constipation (Class D) is usually seen in women and is characterized by presence of numerous prominent and variably sized nuclei in ganglionic areas with active chromatin and faint cytoplasm [2]. Morphologically, our case was not compatible with severe idiopathic constipation. Melanosis coli, characterized by pigment deposition in colonic mucosa after use of certain laxatives, was not seen in the current case, and a toxic or druginduced visceral neuropathy (Class E) may be ruled out in the current case. Hirschsprung s disease, total colonic aganglionosis, and neuronal intestinal dysplasia are categorized as developmental abnormalities (Class C1, C2, and C4) and characterized by segmental absence of ganglion cells, total absence of ganglion cells, and giant ganglia, respectively. Maturational arrest (Class C3) is usually diagnosed in children younger than 1-yr-old. Our case did not fit into any of diseases categorized in Class C. Since no inflammation was noted in the current case, inflammatory sporadic visceral neuropathy (Class B2) can be ruled out. Thus, we believe that our case was most compatible with a non-inflammatory sporadic visceral neuropathy (Class B1). The vacuolated cells were strongly positive for S-100 and weakly positive for synaptophysin, but negative for GFAP and NFP, whereas nerve plexuses (composed of ganglion cells, neurons, and Schwann cells) were positive for all 4 markers. Morphologically the vacuolated cells were incompatible with ganglion cells. The staining profile indicated that the vacuolated cells were most likely proliferative glial cells, since one type of enteric glial cells could
5 Gastrointestinal neuromuscular disorder 147 be negatively stained for GFAP [8]. In a previous study [2], proliferative glial cells were considered in the sporadic type of visceral neuropathy but no antibody stains were performed. The vacuolated cells were also weakly but positively stained for synaptophysin, and negatively stained for NFP, implying that there were some axonal contents in the vacuolated cell region, but the axonal function might have been lost. Calretinin is a calcium-binding protein that is involved in the physiological buffering of excess calcium ions. Calretinin affects cytosolic calcium ions, and calcium transport, and it protects against calcium ion overload. In its absence, accumulation of excess calcium ions inside the cytoplasm causes hyperexitability, which often leads to neurodegeneration [9]. In absence of normal ganglion cells, nerve fibers are usually stained negatively in patients with Hirschsprung s disease [10]. In our case, calretinin, which showed positivity in the submucosal ganglion cells, was negatively stained in myenteric ganglion cells and the vacuolated areas, presumably indicating dysfunction of myenteric ganglion cells and absence of transmission of nerve signals into the muscularis mucosae and muscularis propria. The interstitial cells of Cajal are distributed throughout the gastrointestinal tract and are thought to be pacemaker cells that control the neural and muscular intestinal activity [11]. In the present case there was reduction of staining for CD117 in muscularis propria (5 nuclei per mm 2 ), compared to the normal abundance of interstitial cells of Cajal (18.8 ±3.3 nuclei per mm 2 ) in muscularis propria [11]. The decline in these cells may represent a primary colonic defect or may be secondary to extensive infiltration of the vacuolated cells in muscularis propria. We speculate that the reduced number of interstitial cells of Cajal may also account for the dysmotility problem in the present case. In our case, there was a moderate amount of fibrosis as shown by the trichrome stain, a pattern seen in visceral myopathy. Clearly, there is evidence of severe damage to the neuromuscular apparatus. Additionally the extensive vacuolated S-100 positive cells indicate glial cell proliferation. Such a combination of visceral and neural myopathy has not been documented in the literature; some differences exist between our case and the previously described entities within the sporadic visceral neuropathy category [2]. In conclusion, our case showed extensive proliferation of enteric glial cells and loss of axonal function with diminished positivity for synaptophysin and negative staining for NFP and calretinin, which resulted in colonic pseudo-obstruction. This case is most consistent with a sporadic visceral neuropathy with secondary fibrosis in the muscularis propria. Acknowledgements The authors thank Dr. Donald A. Antonioli, Department of Pathology, Beth Israel Deaconess Medical Center, Boston, MA, and Dr. Frank A. Mitros, Department of Pathology, University of Iowa Medical Center, Iowa City, IA, for expert consultations. References 1. Chokhavatia S, Anuras S. Neuromuscular disease of the gastrointestinal tract. Am J Med Sci 1991;3: Krishnamurthy S, Schuffler MD. Pathology of neuromuscular disorders of the small intestine and colon. Gastroenterology 1987;93: Mann SD, Debinski HS, Kamm MA. Clinical characteristics of chronic idiopathic intestinal pseudoobstruction in adults. Gut 1997;41: Venkatasubramani N, Sood MR. Motility disorders of the gastrointestinal tract. Indian J Pediatr 2006;73: Camilleri M, Carbone LD, Schuffler MD. Familial enteric neuropathy with pseudoobstruction. Dig Dis Sci 1991;36: Coleman LJ, Camilleri M. Chronic intestinal pseudoobstruction: diagnosis and treatment. Mayo Clin Proc 1989;64: Rohrmann CA Jr, Ricci MT, Krishnamurthy S, Schuffler MD. Radiologic and histologic differentiation of neuromuscular disorders of the gastrointestinal tract: visceral myopathies, visceral neuropathies, and progressive systemic sclerosis. Am J Roentegenol 1984;143: Von Boyen GBT, Steinkamp M, Reinshagen M, Schäfer K-H, Adler G, Kirsch J. Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut 2004;53: Heizmann CW. Paraalbumin, intercellular calcium binding protein distribution properties and possible
6 148 Annals of Clinical & Laboratory Science, vol. 38, no. 2, 2008 roles in mammalian cells. Experientia 1984;40: Barshack I, Fridman E, Goldberg I, Chowers Y, Kopolovic J. The loss of calretinin expression indicates aganglionosis in Hirschsrung s disease. J Clin Pathol 2004;57: Wedel T, Spiegler J, Soellner S, Roblick UJ, Schiedeck THK, Bruch H-P, Krammer H-J. Enteric nerve and interstitial cells of Cajal are altered in patients with slowtransit constipation and megacolon. Gastroenterology 2002;123:
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