ESOPHAGEAL MOTOR DYSFUNCTION IN IDIOPATHIC INTESTINAL PSEUDOOBSTRUCTION
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1 GASTROENTEROLOGY 70: , by The Williams & Wilkins Co. Vol. 70, No.5 Printed in U.S.A. ESOPHAGEAL MOTOR DYSFUNCTION IN IDIOPATHIC INTESTINAL PSEUDOOBSTRUCTION MICHAEL D. SCHUFFLER, M.D., AND CHARLES E. POPE, II, M.D. Department of Medicine, University of Washington School of Medicine, the United States Public Health Service Hospital and the Veterans Administration Hospital, Seattle, Washington Five patients with idiopathic intestinal pseudoobstruction were studied with esophageal manometry and all had abnormalities of esophageal motility. In 2, primary peristalsis was replaced by simultaneous contractions and repetitive spontaneous activity was marked. The lower esophageal sphincter failed to relax and the Mecholyl test was positive in both. In the other 3, primary peristalsis was absent, low amplitude simultaneous waves followed swallows, no spontaneous activity was present, and defects in lower esophageal sphincter relaxation were found in two. The Mecholyl test was negative in the one patient tested. The esophagus appears to be abnormal in idiopathic intestinal psemdoobstruction and could prove useful as an organ for diagnostic study in patients who may have this syndrome. Idiopathic intestinal pseudoobstruction (lip) is a chronic illness characterized by symptoms of recurrent intestinal obstruction Exploratory laparotomy is frequently undertaken and although the bowel is noted to be greatly dilated, no obstructing lesion is found. The syndrome is rare and not usually thought of before one or more exploratory laparotomies are done. Bacterial overgrowth often complicates this illness, producing steatorrhea, malnutrition, and sometimes death. To the authors' knowledge, dysphagia has not been reported as a symptom of lip, although two investigators have noted esophageal motor dysfunction on manometric testing. 5, 9 It remains unclear how frequently esophageal motor dysfunction would be present if specifically tested for. The authors have investigated a patient who had dysphagia and who was thought to have achalasia of many years' standing. However, this patient also had obstructive symptoms, steatorrhea, and malnutrition, indicating a more generalized gastrointestinal disease. After appropriate study, it was concluded that he had lip and that the" achalasia" was a part of his syndrome. The authors then investigated 4 other consecutive patients with lip who had no esophageal symptoms to test Received August 13, Accepted November 17, Address requests for reprints to: Charles E. Pope, II, M.D., Chief, Gastroenterology Service, Department of Medicine, Veterans Administration Hospital, 4435 Beacon Avenue South, Seattle, Washington This work was supported by the Postdoctoral Research Training Program in Gastroenterology, National Institute of Arthritis Metabolism and Digestive Diseases-National Institutes of Health Grant 5 T01 AM05099, by Grant 5 R01 AMl6059 from the Public Health Service ("The pathogenesis of human alimentary mucosal disease"), and by Grant 7135 from the Veterans Administration Hospital. A portion of this work was conducted through the Clinical Research Center of the University of Washington supported by Grant RR-37 from the National Institutes of Health. 677 the hypothesis that the esophagus is commonly involved in lip. All 4 proved to have abnormalities of esophageal motor function. Report of Initial Case H. M. was referred to the University of Washington Hospital at the age of 60 with a diagnosis of achalasia. He had developed dysphagia for solids and liquids at age 50 and complained of spending excessive time eating a meal. An esophagogram done by the referring physician was interpreted as showing achalasia; bougie dilations did not improve his dysphagia. Further questioning revealed that he had had intermittent diarrhea since age 20. A barium enema at age 25 showed diverticular disease of the colon. At age 41 the diarrhea became more severe and the patient's weight fell from 130 to 85 pounds. At the age of 43 he had a partial resection of the left colon for diverticular disease. Intermittent abdominal swelling, nausea, and vomiting had been present for many years before his colonic resection. Physical examination showed a pale, cachectic white male who appeared older than his stated age. He had mild abdominal distention and normal bowel sounds. He had an ataxic gait and his deep tendon reflexes were absent. His laboratory studies showed a normal hemogram and sedimentation rate. Liver function tests were normal, the cholesterol was 135 mg per 100 ml, and the serum carotene was 14 U (normal > 100 U). Twentyfour-hour stool fat was 39.6 g on a 100 g per day intake. His B12 absorption with added intrinsic factor was markedly reduced to 0.25 % (normal> 15%). An esophagogram showed absent peristalsis. With the patient upright, the barium formed a column reaching to the aortic arch. The esophagus was slightly dilated and irregular, and spontaneous contractions were marked.
2 678 SCHUFFLER AND POPE Vol. 70, No.. 5 The stomach was normal but the duodenum and jejunum were distended. Excessive fluid was present but no obstructing lesion was found. Barium enema demonstrated striking diverticular disease of the entire colon. The patient's course has been a difficult one. After manometric investigation and an unsuccessful course of bougienage, he was admitted for pneumatic dilation. Before dilation, an Ewald tube was passed to empty the esophagus. His esophagus contracted forcefully and it was impossible to remove the Ewald tube until meperidine and atropine were given. In spite of what appeared to be a technically adequate dilation, the esophagus did not empty well and it was necessary to go through repeated courses of parenteral hyperalimentation in order to maintain the patient's weight. It was difficult to decide whether the main problem was his inability to swallow, his malabsorption, or his recurrent vomiting. Bacterial overgrowth was documented by recovering a large amount of fluid from his proximal small bowel, which contained Escherichia coli, 3 x 10\ Torulopsis glabrata, 1.5 x 10 7, and Propionibacterium, 8 X 10 6 organisms per ml. Small bowel biopsy revealed a mild abnormality of villous architecture, and ganglion cells were present in the submucosa. Significant bacterial overgrowth was confirmed when a course of cloxacillin for an intercurrent skin infection resulted in increases of B12 and fat absorption to 7.3% and 93%, respectively. Over the next 3 years, the patient responded for short periods of time to intermittent antibiotic administration, but repeated hospitalizations were necessary for hyperalimentation. He underwent another pneumatic dilation of the esophagus for worsening dysphagia and weight loss, but without much clinical improvement. A repeat esophagogram demonstrated spontaneous irregular segmental contractions. The stomach emptied slowly and the small intestine was again dilated with no point of mechanical obstruction encountered. Twenty-four hours later, barium was still present in both the stomach and small bowel, and marked segmental contractions causing a to-and-fro movement of barium within the small intestine were observed. He continues to do poorly and it seems likely that periodic hyperalimentation will be necessary to preserve his life. In summary, this man has had a 40-year illness of generalized gastrointestinal smooth muscle dysfunction, which the authors believe fits into the syndrome of lip. In addition, he is the first patient reported with this syndrome to have significant morbidity caused by esophageal motor dysfunction. Patient Population Patients with lip. Clinical information on the 5 patients with IIP is given in table l. J. B. was H. M.'s sister and only sibling. H. M. was unmarried and J. B. was married but without children. H. S. had one sister, her only sibling, who was not studied by us, but who had dysphagia and an aperistaltic esophagus as a child and who needed a gastrojejunostomy to bypass a dilated duodenum as a young adult (Dr. M. G. Clay, personal communication). There were one male and four females. Symptoms of lip had been present for 6 TABLE 1. IIP patients Disease Patient Age Sex duration Wt(kg) (yr) Fat absorption (%of intake) Dysphagia H.M. 60 M Yes J. B. 57 F No H.S. 31 F No D.L. 63 F No K.B. 15 F NDa No and = not done. months to 45 years. Three of the patients had had one or more laparotomies, at which time marked bowel distention was found without an obstructing lesion present. The following additional criteria for the diagnosis of lip were present in these patients: l. Recurrent episodes of abdominal pain and distention associated with vomiting. 2. No evidence for a systemic disease such as scleroderma, amyloidosis, myxedema, etc. Scleroderma was excluded in each patient by the absence of Raynaud's phenomenon and of skin, joint, and heart abnormalities. Each patient had a normal chest roentgenogram. Rectal and small bowel biopsies were obtained from all 5 and were stained with Congo Red. None had amyloid. All had urinalyses and none had proteinuria, red cells, or red cell casts. 3. No evidence for any inflammatory disease of the intestine or of contiguous organs. 4. Small intestinal dilation, often dramatic in appearance, on small bowel series with no mechanical obstruction encountered. 5. Excessive, often voluminous, quantities of fluid contaminated with bacteria obtained by aspiration of the upper small intestine. Patients with secondary pseudoobstruction. To serve as controls, 4 other patients whose illnesses were complicated by secondary pseudoobstruction were studied. Two of them had scleroderma, the 3rd had jejunal diverticulosis, and the 4th had intestinal pseudoobstruction and stasis syndrome secondary to diffuse primary lymphoma of the small bowel. The 4 patients ranged in age from 39 to 68 years (mean 58 years) and 2 were men. Patients with other gastrointestinal diseases. Six consecutive patients with various gastrointestinal problems were selected as additional controls. Three of these had clinically significant malabsorptive disorders (one with malnutrition secondary to intractable malabsorption of unknown etiology, one with postgastrectomy steatorrhea and weight loss, and one with Crohn's disease of the proximal small intestine). Of the remaining 3, one had chronic, recurrent vomiting after vagotomy and gastrojejunostomy for an annular pancreas, one had recurrent vomiting secondary to gastroparesis diabeticorum, and one had malnutrition and nonspecific colitis after a toxic course of amoebic colitis. The 6 patients had an age range of 19 to 70 years (mean, 41 years) and 3 were men. These patients were selected because their illness had some features, i.e., malabsorption, vomiting, or marked weight loss, that are present in lip. The authors wished to make especially certain that these features did not by themselves influence esophageal motor function. These studies were approved by the Human Subjects Review Committee of the University of Washington and all patients gave informed consent.
3 May 1976 ESOPHAGUS IN INTESTINAL PSEUDOOBSTRUCTION 679 Methods Before manometry, all 5 patients with lip had esophagograms with standard barium suspensions. After an overnight fast, patients swallowed a four-lumen polyvinyl catheter whose total outside diameter was 6 mm. The esophageal body was not emptied of retained fluid. The openings were 2 mm in diameter and were located with the proximal lumen 15 cm from the end of the catheter, two middle openings 10 cm from the end of the catheter, and a distal opening 5 cm from the end of the catheter. The catheters were infused by a constant infusion pump at a rate 0(2.4 ml per min. In two cases, a Honeywell 31 motility probe was used instead of the infused catheters. In control experiments, peristaltic amplitudes and lower esophageal sphincter (LES) pressures recorded by the two systems were comparable. Mter a stepwise withdrawal of the proximal and two middle catheters through the region of the lower esophageal sphincter, with swallowing at each station to identify the presence or absence of sphincter relaxation, four rapid pull-throughs were done with the two middle tips, and the amplitudes of the recorded sphincter profile were averaged to obtain a value for LES pressure. Peristaltic amplitudes were calculated from five swallows at each 2-cm station from one end of the esophagus to the other. Mecholyl tests were done according to the method of Kramer and Ingelfinger, using a balloonkymograph. 12 Initial doses of Mecholyl were 0.5 ing and the dose was raised incrementally until a positive result (complete luminal obliteration) was obtained or until 5 mg of Mecholyl had been given. Results Four of the 5 patients with IIP had abnormal esophageal motor function observed on barium swallow (table 2). All 5 had manometric abnormalities of the esophagus. There was variability in the types of motor dysfunction recorded (table 2). Primary peristalsis was absent in each patient with IIP. In 2 (H. M. and J. B.), it was absent throughout the entire esophagus. In the other 3, it was absent in only the lower two-thirds. Four of the 5 patients had low amplitude simultaneous waves after swallows (figure 1). The 5th patient's (J. B.) marked spontaneous activity made it difficult to determine whether any of the waves were produced by swallowing. Two of the patients (H. M. and J. B.) had repetitive waves after swallows and marked spontaneous and repetitive activity between swallows in the lower onethird of the esophagus (Fig. 2). This spontaneous activity was atypical of diffuse spasm or active achalasia because the waves recorded simultaneously at two different sites were always out of phase. 13 The other 3 patients did not have spontaneous activity. LES pressures ranged from 10 to 54 mm Hg (mean 28 mm Hg). The LES pressure in H. M. was measured some time after pneumatic dilation and was therefore probably lower than it had been. (This mean LES pressure of 28 compares with a mean of 48.3 mm Hg that has been recorded in achalasia). Abnormalities of sphincter relaxation occurred in 4 patients; 3 had no relaxation and the 4th had partial relaxation. Mecholyl tests were positive in 2 of 3 patients tested (H. M. and J. B.). Both had flushing and salivation after Mecholyl, but neither developed small bowel symptoms. These two patients had classic findings of achalasia consisting of aperistalsis, failure of sphincter relaxation, and positive Mecholyl tests. However, they had atypical findings as well. They lacked primary peristalsis in the most proximal portion of the esophagus and their marked spontaneous activity was always out of phase as measured at two different recording sites at the same time. A 3rd patient (H. S.) was not tested with Mecholyl but her lack of primary peristalsis coupled with failure of LE$ relaxation is consistent with the diagnosis of achalasia. The other 2 patients had motility recordings not classical in achalasia because in one the LES relaxed normally and in the other the Mecholyl test was negative. Neither of these studies was typical of scleroderma because both had high sphincter pressures and simultaneous nonperistal tic waves followed swallows. 14, 15 Of the 4 control patients with diseases complicated by secondary pseudoobstruction (table 3), one (L. C.) had classic manometric findings of scleroderma with complete absence of esophageal waves and a very low LES pressure. The second patient with presumptive scleroderma (dilated small intestine, pulmonary fibrosis, and subungual telangiectasis) had primary peristaltic waves of low amplitude and a negative Mecholyl test, findings consistent with scleroderma. The other 2 in this group TABLE 2. Patients with IIP Esophageal manometry Patient LES LES Primary peristalsis Simultaneous Mecholyl Spontaneous pressure relaxa waves after activity test (mmhg) tion Lower 1/:1 Upper II:! swallows (mg)" Esophageal radiography H.M. 16 No Absent Absent Yes 4+ + Nonperistaltic spontaneous (lower 1/3) (0.5) contractions with slow emptying; air fluid level J.B. 33 No Absent Absent Yes 3+ + Excess fluid; non peristaltic (lower 11.1) (2) spontaneous contractions H.S. 10 No Absent Present Occasional No ND Normal D.L. 30 Yes Absent Present Yes No ND Aperistalsis; dilation (low amplitude) K.B. 50 Partial Absent Present Occasional No Neg. Aperistalsis (low amplitude) a + = positive; ND = not done; Neg. = negative. In parentheses is the amount of Mecholyl given (mg).
4 680 SCHUFFLER AND POPE Vol. 70, No..5 Discussion Esophageal aperistalsis has been demonstrated in all 5 patients with lip in this study. Two 'Of the patients (H. M. and J. B.) had manometric findings that were virtually indistinguishable from "vigorous" achalasia. 13 The other 3 had tracings consistent with but not classical for achalasia. Esophageal motility testing was done in 5 previously reported cases of IIP 5 9 and was abnormal in 4. No uniform manometric abnormality was 'apparent in review of the 4 cases. Although 2 were completely aperistaltic, a 3rd had intermittently normal peristalsis, and the 4th had long duration, high amplitude, repetitive contractions. This data confirms that esophageal motor dysfunction is common in lip, and suggests that this esophageal abnormality is part of a more diffuse gastrointestinal motor disorder. It is not surprising that a uniform pattern of esophageal motor dysfunction in lip could not be defined. There is little known about the pathology of this syndrome. Although a lesion of the myenteric plexus had been described in one case,6 lip could possibly be the end result of several different etiologies, pathologies, and pathophysiologies. Each could conceivably produce a RESPIRATION SWALLOW PROXIMAL MIDDLE-I MIDDLE-2 H,M. DISTAL ~ IOsee FIG. 1. Simultaneous contractions of esophageal body after swallowing. The top channel monitors respiration, inspiration producing a downward deflection. Swallowing is shown on the second tracing. The tracing labeled "proximal" is 25 cm from the teeth; the two tracings labeled Middle-l and Middle-2 are 30 cm from the teeth; the distal tip is 35 cm from the teeth. Swallowing produces a broad, low amplitude simultaneous wave in all leads. PROXIMAL MIDDLE" (G. G. and D. H.) had normal esophageal function, with the exception of an occasional simultaneous wave in G. G. Of the 6 other control patients (table 3), 5 had perfectly normal esophageal motility. The 6th (L. U.) had many aperistaltic swallows, absence of sphincter relaxation, and occasional simultaneous waves after swallows. This patient had an intractable malabsorptive disorder of unknown etiology which eventually caused his death. He did not have any clinical or X-ray evidence of pseudoobstruction. The one feature of his motility study which differentiated him from the lip patients was the occasional occurrence of a perfectly normal peristaltic wave. This contrasts with the lip patients, who never had peristaltic waves. The one control patient with occasional spontaneous waves (J. B.) was 70 years of age. This finding may occasionally be present in normal people. 16 MIDDLE-2 DISTAL ~ IOsee 2. Spontaneous activity of esophageal body. The proximal tip is 32 cm from the teeth, the two middle tips are 37 cm from the teeth, and the distal tip is 42 cm from the teeth. The distal tip is located in the upper portion of the LES, and most of the pressure variations are related to respiration. It can be seen that there are different rates of spontaneous contractions 5 cm and 10 cm above the LES. The patient has not swallowed during this period, as shown by the flat record from the swallow marker. FIG.
5 May 1976 ESOPHAGUS IN INTESTINAL PSEUDOOBSTRUCTION 681 TABLE 3. Esophageal manometry LES LES Primary peristalsis Simultaneous Patient pressure relaxa- waves after (mmhg) tion Lower 2f3 Upper V3 swallows Spontaneous activity Mecholyl testa Patients with secondary pseudoobstruction G.G. 24 Yes Present M.S-P. 10 No Present (low amplitude) L. C. 3.5 Yes Absent D.H. 28 Yes Present Patients with other gastrointestinal diseases L.U. 7 No Infrequent J. B. 26 Yes Present D.O. 27 Yes Present R.McD. 17 Yes Present K.S. 6 Yes Present C.K. 25 Yes Present Present Occasional No ND Present No No Neg. Present Occasional No ND Present No Occasional ND a ND ~ not done; neg. ~ negative. somewhat different manometric pattern_ In addition, these patterns might vary with the natural history of the disease_ Serial manometric examinations were not done on patients in this study, but would be of interest_ The authors tried to be cautious when setting up criteria for the diagnosis of lip. Any patient who had any evidence at all suggestive of Raynaud's phenomenon or of scleroderma was specifically excluded, although it is recognized that scleroderma has been reported as an isolated disease of the gastrointestinal tracl It is unlikely, however, that any of these lip patients had isolated gastrointestinal scleroderma_ None of them had manometric findings of scleroderma, which usually consist of weak or absent peristaltic waves and a low LES pressure In contrast, the 2 patients with pseudoobstruction secondary to scleroderma had manometries quite characteristic of this disease. Because chronic vomiting, malabsorption, and marked weight loss were universally present in the patients with lip, 6 consecutive patients with one or more of these symptoms were chosen to serve as controls_ All had primary peristaltic waves which were of normal amplitude and duration. Although L. U. had many aperistaltic swallows, some were normally peristaltic. The patients with lip differed in that they were consistently aperistaltic. lip is a rare and poorly defined syndrome which is often difficult to diagnose. When a patient with abdominal pain and vomiting has X-rays showing small intestinal dilation, one rightfully thinks of organic obstruction_ If, however, symptoms have extended over many months and years and if, in particular, the patient has had one or more unrevealing laparotomies, lip should be considered_ Esophageal manometry may prove to be a useful test in this situation, because a normal test would tend to make lip an unlikely diagnosis_ Conversely, a manometry consistent with either classical or atypical achalasia in a patient with idiopathic small bowel dilation should suggest the diagnosis of lip. The present observations in lip need to be extended to a greater number of patients to determine the frequency and types of esophageal involvement in this syndrome. If these findings are confirmed, it will indicate that lip is a more diffuse disease of the gut than is generally recognized. It will also lend support to the use of esophageal manometry in helping to diagnose or exclude this syndrome in patients with chronic obstructive symptoms. REFERENCES 1. N;iish JM, Capper WM, Brown NJ: Intestinal pseudo-obstruction with steatorrhea. Gut 1:62-66, McClelland HA, Lewis MJ, Naish JM: Idiopathic steatorrhe-a with intestinal pseudo-obstruction. Gut 3: , Paul CA, Tomujasu U, Mellinkoff SM: Nearly fatal pseudoobstruction of the small intestine. A case report of its relief by subtotal resection of the small bowel. Gastroenterology 40: , Murley RS: Painful enteromegaly of unknown etiology. Proc R Soc Med 52: , Maldonado JE, Gregg JA, Green PA et al: Chronic idiopathic intestinal pseudo-obstruction. Am J Med 49: , Dyer NH, Dawson AM, Smith BF et al: Obstruction of bowel due to lesion in the myenteric plexus. Br Med J 1: , Nahai F: Pseudo-obstruction of the small bowel. Bristol Med Chir J 84: , Pearson AJ, Brzechwa-Ajdukiewicz, McCarthy CF: Intestinal pseudoobstruction with bacterial overgrowth in the small intestine. Am J Dig Dis 14: , Moss AA, Goldberg HI, Brotman M: Idiopathic intestinal pseudoobstruction. Am J Roentgenol Radium Ther Nucl Med 115: , Cockel R, Hill EE, Rushton DI, et al: Familial steatorrhea with calcification of the basal ganglia and mental retardation. Q J Med 42: , Taybi H, Keele D: Hypoparathyroidism: A review of the literature and report of two cases in sisters, one with steatorrhea and intestinal pseudo-obstruction. Am J Roentgenol 88: , Kramer P, Ingelfinger FJ: Esophageal sensitivity to Mecholyl in cardiospasm. Gastroenterology 19: , Sanderson DR, Ellis FH, Schlegel JF et al: Syndrome of vigorous achalasia: Clinical and physiologic observations. Dis Chest 52: , 1967
6 682 SCHUFFLER AND POPE Vol. 70, No Creamer B, Anderson HA, Code CF: Esophageal motility in patients with scleroderma and related diseases. Gastroenterologia 86: , Atkinson M, Summerling MD: Oesophageal changes in systemic sclerosis. Gut 7: , Nagler R, Spiro HM: Serial esophageal motility studies in asymptomatic young subjects. Gastroenterology 41 : , Rodnan GP, Fennell RH, Jr: Progressive systemic sclerosis sine scleroderma. JAMA 180: , Horswell RR, Hargrove MD, Peete WP et al: Scleroderma presenting as malabsorption syndrome. Gastroenterology 40: , Crown S: Visceral scleroderma without skin involvement. Br Med J 2: , Treacy WL, Baggenstoss AH, Slocumb CH, et al: Scleroderma of the esophagus. A correlation of histologic and physiologic findings. Ann Intern Med 59: , 1963
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