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Jejunal Trauma Following Perfusion of the Small Intestine in Nontropical Sprue
Vol. 54, No.3 Printed in U.S.A.
GASTROENTEROLOGY
Copyright © 1968_by_The Williams & Wilkins Co.
JEJUNAL TRAUMA FOLLOWING PERFUSION OF THE SMALL INTESTINE IN NONTROPICAL SPRUE WALTER W.
H. J.
C.
SCHMID,
M.D., SIDNEY F. D.M.
PHILLIPS,
M.D.,
AND
SUMMERSKILL,
Mayo Clinic and Mayo Foundation: Gastroenterology Unit and Section of Medicine (Drs. Phillips and Summerskill), Mayo Graduate School of Medicine (University of Minnesota) (Dr. Schmid), Rochester, Minnesota
plied above and below the balloon at the pressure of 70 mm of mercury. At the conclusion of the study, the balloon is deflated before manual retrieval of the tube.
The purpose of this paper is to describe perforation of the small intestine and the features consistent with penetration that followed perfusion studies of the jejunum in 2 patients with nontropical sprue. One or more of several components of the technique may have been the traumatic agent. The report is particularly relevant since perfusion, now a standard method of studying absorptive function, is being applied to small series of patients with nontropical sprue,l,2 and attention recently has been drawn to a tendency to spontaneous perforation of the small bowel in this condition. 3
Results
Evidence of acute trauma to an intraabdominal viscus occurred immediately after perfusion on two of the 138 occasions in which the technique had been employed (table 1). In both instances, the patient had nontropical sprue and the disease was in partial or complete remission. Neither patient had evidence of associated conditions believed to cause perforation. A comparable number of patients with other diseases (the great majority having cirrhosis, regional enteritis, or ulcerative colitis) experienced no complications with the procedure, and a much larger number of healthy volunteers also underwent the studies uneventfully. In both patients, complications occurred after perfusion of isotonic solutions containing various concentrations of potassium, sodium, chloride, and bicarbonate to which phenolsulfonphthalein had been added as a reference marker. This technique, applied either to the jejunum or ileum, has been used extensively in our clinic for studying transport of these electrolytes or of ammonia. 5 , 6
Materials and Methods
The method of perfusion has been described previously in detail.'-· In summary, it involves peroral intubation with a composite tube (diam 6 mm), made from four lengths of polyvinyl tubing cemented with tetrahydrofuran, to which a latex (Sawyer) balloon is attached. A terminal finger cot contains 3 ml of mercury to facilitate spontaneous advancement; after positioning in the small intestine under fluoroscopic control, the balloon is inflated to a diameter of 4.4 em with 50 ml of water to occlude the lumen of the gut and to prevent contamination of the segment under study.' Solutions are perfused at a rate of 10 ml per min immediately distal to the balloon. Suction (Gomco pump) is apReceived August 7, 1967. Accepted October 21, 1967. Address requests for reprints to: Section of Publications, Mayo Clinic, Rochester, Minnesota 55901. This investigation was supported in part by Research Grant AM-6908 and Training Grant T1-AM-5259 from the National Institutes of Health, Public Health Service.
417
Report of Cases
Case 1. A 61-year-old woman had experienced symptoms consistent with malabsorption since 1931. Nontropical sprue was diagnosed in 1959, based upon a high 24-hr fecal fat excretion (50 g), decreased levels of carotene and calcium in the blood, radiological features in the small intestine of malabsorption, and the
418
CASE REPORTS TABLE
1. Complications of small intestinal perfusion
Subjects
No. of studies
Complications
Nontropical sprue. . . . . . . . . Other diseases. . . . . . . . . . . . . Healthly volunteers. . . . . . .
23 23 92
o o
Total. . ...................
138
2
2
characteristic appearance of the jejunal biopsy specimen. After a gluten-restricted diet was prescribed, she had complete remission of her symptoms and gained 13 lb. At the time of small bowel perfusion in November 1966, the fecal fat excretion was 8 g in 24 hr and the serum carotene concentration was normal; there had been no definite change in the histological appearance of the jejunum. During perfusion of the lower jejunum with two isotonic solutions (containing in milliequivalents per liter: sodium, 140 or 95; potassium, 10 or 55; chloride, 115 or 80; and bicarbonate, 35 or 70), the patient experienced colicky abdominal pain, which continued after the study was terminated. On the following day, the abdomen was distended and diffusely tender to palpation. The patient was nauseated and febrile (temperature 102 F), and had a mild leukocytosis (leukocyte count 12,500 per mm", 96% neutrophils). On the 2nd day, the pain was localized to the left of the umbilicus and was associated with rebound tenderness and vomiting. A roentgenogram of the abdomen revealed a dilated loop of small bowel. Use of a conservative regimen resulted in the patient's improvement and, 1 week later, barium studies of the small intestine showed a walled off perforation of the lower portion of the jejunum (fig. 1). The patient's subsequent recovery was uneventful. Case 2. A 51-year-old woman first experienced symptoms consistent with intestinal malabsorption in 1940. In 1959 a diagnosis of nontropical sprue was made on the basis of an excessive 24-hr fecal fat excretion of 55 g; reduced serum concentrations of carotene, calcium, and albumin; radiographic evidence of malabsorption; and characteristic appearance of a jejunal biopsy specimen. Since then, the patient experienced partial remission while taking a gluten-restricted diet and had gained 10 lb. At the time of special studies in August 1966, the fecal fat excretion was 23 g in 24 hr, the serum carotene concentration was 24
Vol. 54, No.3
units per 100 ml, and another jejunal biopsy specimen revealed no change. During a 90-min period of perfusion of the jejunum with isotonic solutions containing glucose or mannitol (140 mM), sodium chloride (60 mEq per liter), and potassium bicarbonate (20 mEq per liter), mild colicky abdominal pain developed. The pain continued after the study was finished and, the following day, abdominal distention, slight generalized rebound tenderness, and decreased bowel sounds were associated with a temperature of 100 F and radiological appearances consistent with ileus (fig. 2). A diagnosis of traumatic penetration or perforation of the small intestine was made, and conservative treatment was instituted. During the following 3 days, the symptoms subsided and the roentgenographic appearance returned to normal. The patient was dismissed from the hospital and has remained well since.
Discussion
A causal relationship between the perfusion procedure and the abdominal complications is proposed because of the close time relationship involved in each case; which aspect of the perfusion study was responsible is less evident. Penetration or perforation of the small intestine by the tips of tubes is rare 7 and usually occurs only with advanced intestinal disease, such as prolonged bowel obstruction. s An unusual complication, occasioned by suction, is necrosis of the intestinal wall from aspiration of the mucosa into the suction holes of the tube. 9 Intussusception of the small intestine also may occur occasionally with intubation 10 , 11 and might be anticipated more frequently in patients with sprue, since in some this complication may develop spontaneously.1 2 ,13 A further consideration is the possibility that trauma to the small intestine, including hematoma, could be due to inflation of the balloon. The volume contained by the balloon and which is necessary to elicit a satisfactory stretch response of the intestine so that effective occlusion of the lumen could be achieved had been determined in earlier studies. 4 However, balloons inflated under greater pressure are an accepted cause of trauma resulting from esophageal tamponade,14 and balloon inflation has been in-
March 1968
419
CASE REPORTS
FIG. 1. Case 1. Roentgenogram of small intestine showing walled off perforation of lower portion of jejunum. FIG. 2. Case 2. Roentgenogram of abdomen showing dilated small intestine.
criminated as a cause of intussusception during use of the Miller-Abbott tubeY The Sawyer balloon has been extensively used, without complications, by our group in studies of antral motility. IS Finally, the possible effects of the potassium contained in the perfusion solutions deserve attention. Both studies included a 3D-min period of perfusion with isotonic solutions containing 55 and 20 mEq per liter of potassium, respectively. Inflammatory damage (including ulceration and perforation) of the small intestine due to potassium is well documented 16 , 17 and has been attributed to tablet preparations; recently,lS potassium in liquid form has been associated with jejunal ulceration. However, intestinal perfusion in dogs 19 and man 5 with isotonic (154 mM) potassium chloride has not produced complications or evidence of bleeding into the bowel (S. F. Phillips and W. H. J. Summerskill, unpublished data). Traumatic complications of perfusion techniques have not been reported. AI-
though the cause of trauma in these 2 patients cannot be identified, it appears likely from the absence of such complications in the large number of individuals with other conditions studied that patients with nontropical sprue may run a special risk when undergoing intubation procedures. Ulceration and perforation of the small bowel, which is often fatal, may occur spontaneously in sprue, and the possible reasons for this have been reviewed. 3 In a few instances, a susceptibility of the small intestine to trauma, even when the disease is in partial or complete remission, is implied by our experiences. Awareness of this possibility is important, since with immediate routine conservative treatment both of our patients recovered uneventfully. Summary
Evidence of trauma to the Jejunum occurred after small bowel perfusion studies in 2 patients with nontropical sprue. No
420
CASE REPORTS
complications followed the procedure in 115 healthy volunteers or patients with other diseases. Likely causes of trauma involved in the method are reviewed, and the susceptibility of patients with nontropical sprue to complications is considered. REFERENCES 1. Fordtran, J. S., F. C. Rector, T. W. Locklear, and M. F. Ewton. 1967. Water and solute movement in the small intestine of patients with sprue. J. Clin. Invest. 46: 287298. 2. Schmid, W. C., S. F. Phillips, and W. H. J. Summerskill. 1967. Jejunal transport of electrolytes and water in non-tropical sprue (abstr.). Clin. Res. 15: 243. 3. Bayless, T. M., R. F. Kapelowitz, W. M. Shelley, W. F. Ballinger, II, and T. R. Hendrix. 1967. Intestinal ulceration-a complication of celiac disease. New Eng. J. Med. 276: 996--1002. 4. Phillips, S. F., and W. H. J. Summerskill. 1966. Occlusion of the jejunum for intestinal perfusion in man. Proc. Mayo Clin. 41: 224-231. 5. Phillips, S. F., and W. H. J. Summerskill. 1966. Comparison of electrolyte transport in relation to intraluminal concentrations in the human jejunum and ileum (abstr.). J. Clin. Invest. 45: 1056. 6. Ewe, K., and W. H. J. Summerskill. 1965. Transfer of ammonia in the human jejunum. J. Lab. Clin. Med. 65: 839-847. 7. Smith. B. C. 1945. Experiences with the Miller-Abbott tube: a statistical study of 1,000 cases. Ann. Surg. 122: 253-259. 8. Berger, L., and S. Achs. 1947. Perforation of the small intestine by the Miller-Abbott tube. Surgery 22: 648-656.
Vol. 54, No.3
9. Bockus, H. L. 1964. Gastroenterology, Ed. 2, Vol. II, p. 67. W. B. Saunders Company, Philadelphia. 10. McGoon, D. C. 1956. Intussusception: a hazard of intestinal intubation. Surgery 40: 515-519. 11. Sower, N., and G. P. Wratten. 1965. Intussusception due to intestinal tubes: case reports and review of literature. Amer. J. Surg.ll0: 441-444. 12. Bloch, C., and H. M. Peck. 1964. Radiological notes: transient intussusception in sprue. J. Mount Sinai Hosp. N. Y. 31: 236-241. 13. Cortell, S., E. E. Rieber, T. W. Sheehy, and M. E. Conrad. 1967. Tropical sprue and intussusception: an unusual complication: report of a case. Amer. J. Dig. Dis. 12: 216-221. 14. Read, A. E., A. M. Dawson, D. N. S. Kerr, M. D. Turner, and S. Sherlock. 1960. Bleeding oesophageal varices treated by oesophageal compression tube. Brit. Med. J. 1: 227-231. 15. Garrett, J. M., W. H. J. Summerskill, and C. F. Code. 1966. Antral motility in patients with gastric ulcer. Amer. J. Dig. Dis. 11: 780-789. 16. Baker, D. R., W. H. Schrader, and C. R. Hitchcock. 1964. Small-bowel ulceration apparently associated with thiazide and potassium therapy. J. A. M. A.190: 586--590. 17. Lawrason, F. D., E. Alpert, F. L. Mohr, and F. G. McMahon. 1965. Ulcerative-obstructive lesions of the small intestine. J. A. M. A. 191: 641-644. 18. Warr, O. S., and J. P. Nash. 1967. Jejunal ulceration: report of a case apparently associated with potassium gluconate. J. A. M.A. 199: 217-218. 19. Phillips, S. F., and C. F. Code. 1966. Sorption of potassium in the small and large llltestine. Amer. J. Physiol. 211: 607-613.
GASTROENTEROLOGY
Copyright © 1968_by_The Williams & Wilkins Co.
JEJUNAL TRAUMA FOLLOWING PERFUSION OF THE SMALL INTESTINE IN NONTROPICAL SPRUE WALTER W.
H. J.
C.
SCHMID,
M.D., SIDNEY F. D.M.
PHILLIPS,
M.D.,
AND
SUMMERSKILL,
Mayo Clinic and Mayo Foundation: Gastroenterology Unit and Section of Medicine (Drs. Phillips and Summerskill), Mayo Graduate School of Medicine (University of Minnesota) (Dr. Schmid), Rochester, Minnesota
plied above and below the balloon at the pressure of 70 mm of mercury. At the conclusion of the study, the balloon is deflated before manual retrieval of the tube.
The purpose of this paper is to describe perforation of the small intestine and the features consistent with penetration that followed perfusion studies of the jejunum in 2 patients with nontropical sprue. One or more of several components of the technique may have been the traumatic agent. The report is particularly relevant since perfusion, now a standard method of studying absorptive function, is being applied to small series of patients with nontropical sprue,l,2 and attention recently has been drawn to a tendency to spontaneous perforation of the small bowel in this condition. 3
Results
Evidence of acute trauma to an intraabdominal viscus occurred immediately after perfusion on two of the 138 occasions in which the technique had been employed (table 1). In both instances, the patient had nontropical sprue and the disease was in partial or complete remission. Neither patient had evidence of associated conditions believed to cause perforation. A comparable number of patients with other diseases (the great majority having cirrhosis, regional enteritis, or ulcerative colitis) experienced no complications with the procedure, and a much larger number of healthy volunteers also underwent the studies uneventfully. In both patients, complications occurred after perfusion of isotonic solutions containing various concentrations of potassium, sodium, chloride, and bicarbonate to which phenolsulfonphthalein had been added as a reference marker. This technique, applied either to the jejunum or ileum, has been used extensively in our clinic for studying transport of these electrolytes or of ammonia. 5 , 6
Materials and Methods
The method of perfusion has been described previously in detail.'-· In summary, it involves peroral intubation with a composite tube (diam 6 mm), made from four lengths of polyvinyl tubing cemented with tetrahydrofuran, to which a latex (Sawyer) balloon is attached. A terminal finger cot contains 3 ml of mercury to facilitate spontaneous advancement; after positioning in the small intestine under fluoroscopic control, the balloon is inflated to a diameter of 4.4 em with 50 ml of water to occlude the lumen of the gut and to prevent contamination of the segment under study.' Solutions are perfused at a rate of 10 ml per min immediately distal to the balloon. Suction (Gomco pump) is apReceived August 7, 1967. Accepted October 21, 1967. Address requests for reprints to: Section of Publications, Mayo Clinic, Rochester, Minnesota 55901. This investigation was supported in part by Research Grant AM-6908 and Training Grant T1-AM-5259 from the National Institutes of Health, Public Health Service.
417
Report of Cases
Case 1. A 61-year-old woman had experienced symptoms consistent with malabsorption since 1931. Nontropical sprue was diagnosed in 1959, based upon a high 24-hr fecal fat excretion (50 g), decreased levels of carotene and calcium in the blood, radiological features in the small intestine of malabsorption, and the
418
CASE REPORTS TABLE
1. Complications of small intestinal perfusion
Subjects
No. of studies
Complications
Nontropical sprue. . . . . . . . . Other diseases. . . . . . . . . . . . . Healthly volunteers. . . . . . .
23 23 92
o o
Total. . ...................
138
2
2
characteristic appearance of the jejunal biopsy specimen. After a gluten-restricted diet was prescribed, she had complete remission of her symptoms and gained 13 lb. At the time of small bowel perfusion in November 1966, the fecal fat excretion was 8 g in 24 hr and the serum carotene concentration was normal; there had been no definite change in the histological appearance of the jejunum. During perfusion of the lower jejunum with two isotonic solutions (containing in milliequivalents per liter: sodium, 140 or 95; potassium, 10 or 55; chloride, 115 or 80; and bicarbonate, 35 or 70), the patient experienced colicky abdominal pain, which continued after the study was terminated. On the following day, the abdomen was distended and diffusely tender to palpation. The patient was nauseated and febrile (temperature 102 F), and had a mild leukocytosis (leukocyte count 12,500 per mm", 96% neutrophils). On the 2nd day, the pain was localized to the left of the umbilicus and was associated with rebound tenderness and vomiting. A roentgenogram of the abdomen revealed a dilated loop of small bowel. Use of a conservative regimen resulted in the patient's improvement and, 1 week later, barium studies of the small intestine showed a walled off perforation of the lower portion of the jejunum (fig. 1). The patient's subsequent recovery was uneventful. Case 2. A 51-year-old woman first experienced symptoms consistent with intestinal malabsorption in 1940. In 1959 a diagnosis of nontropical sprue was made on the basis of an excessive 24-hr fecal fat excretion of 55 g; reduced serum concentrations of carotene, calcium, and albumin; radiographic evidence of malabsorption; and characteristic appearance of a jejunal biopsy specimen. Since then, the patient experienced partial remission while taking a gluten-restricted diet and had gained 10 lb. At the time of special studies in August 1966, the fecal fat excretion was 23 g in 24 hr, the serum carotene concentration was 24
Vol. 54, No.3
units per 100 ml, and another jejunal biopsy specimen revealed no change. During a 90-min period of perfusion of the jejunum with isotonic solutions containing glucose or mannitol (140 mM), sodium chloride (60 mEq per liter), and potassium bicarbonate (20 mEq per liter), mild colicky abdominal pain developed. The pain continued after the study was finished and, the following day, abdominal distention, slight generalized rebound tenderness, and decreased bowel sounds were associated with a temperature of 100 F and radiological appearances consistent with ileus (fig. 2). A diagnosis of traumatic penetration or perforation of the small intestine was made, and conservative treatment was instituted. During the following 3 days, the symptoms subsided and the roentgenographic appearance returned to normal. The patient was dismissed from the hospital and has remained well since.
Discussion
A causal relationship between the perfusion procedure and the abdominal complications is proposed because of the close time relationship involved in each case; which aspect of the perfusion study was responsible is less evident. Penetration or perforation of the small intestine by the tips of tubes is rare 7 and usually occurs only with advanced intestinal disease, such as prolonged bowel obstruction. s An unusual complication, occasioned by suction, is necrosis of the intestinal wall from aspiration of the mucosa into the suction holes of the tube. 9 Intussusception of the small intestine also may occur occasionally with intubation 10 , 11 and might be anticipated more frequently in patients with sprue, since in some this complication may develop spontaneously.1 2 ,13 A further consideration is the possibility that trauma to the small intestine, including hematoma, could be due to inflation of the balloon. The volume contained by the balloon and which is necessary to elicit a satisfactory stretch response of the intestine so that effective occlusion of the lumen could be achieved had been determined in earlier studies. 4 However, balloons inflated under greater pressure are an accepted cause of trauma resulting from esophageal tamponade,14 and balloon inflation has been in-
March 1968
419
CASE REPORTS
FIG. 1. Case 1. Roentgenogram of small intestine showing walled off perforation of lower portion of jejunum. FIG. 2. Case 2. Roentgenogram of abdomen showing dilated small intestine.
criminated as a cause of intussusception during use of the Miller-Abbott tubeY The Sawyer balloon has been extensively used, without complications, by our group in studies of antral motility. IS Finally, the possible effects of the potassium contained in the perfusion solutions deserve attention. Both studies included a 3D-min period of perfusion with isotonic solutions containing 55 and 20 mEq per liter of potassium, respectively. Inflammatory damage (including ulceration and perforation) of the small intestine due to potassium is well documented 16 , 17 and has been attributed to tablet preparations; recently,lS potassium in liquid form has been associated with jejunal ulceration. However, intestinal perfusion in dogs 19 and man 5 with isotonic (154 mM) potassium chloride has not produced complications or evidence of bleeding into the bowel (S. F. Phillips and W. H. J. Summerskill, unpublished data). Traumatic complications of perfusion techniques have not been reported. AI-
though the cause of trauma in these 2 patients cannot be identified, it appears likely from the absence of such complications in the large number of individuals with other conditions studied that patients with nontropical sprue may run a special risk when undergoing intubation procedures. Ulceration and perforation of the small bowel, which is often fatal, may occur spontaneously in sprue, and the possible reasons for this have been reviewed. 3 In a few instances, a susceptibility of the small intestine to trauma, even when the disease is in partial or complete remission, is implied by our experiences. Awareness of this possibility is important, since with immediate routine conservative treatment both of our patients recovered uneventfully. Summary
Evidence of trauma to the Jejunum occurred after small bowel perfusion studies in 2 patients with nontropical sprue. No
420
CASE REPORTS
complications followed the procedure in 115 healthy volunteers or patients with other diseases. Likely causes of trauma involved in the method are reviewed, and the susceptibility of patients with nontropical sprue to complications is considered. REFERENCES 1. Fordtran, J. S., F. C. Rector, T. W. Locklear, and M. F. Ewton. 1967. Water and solute movement in the small intestine of patients with sprue. J. Clin. Invest. 46: 287298. 2. Schmid, W. C., S. F. Phillips, and W. H. J. Summerskill. 1967. Jejunal transport of electrolytes and water in non-tropical sprue (abstr.). Clin. Res. 15: 243. 3. Bayless, T. M., R. F. Kapelowitz, W. M. Shelley, W. F. Ballinger, II, and T. R. Hendrix. 1967. Intestinal ulceration-a complication of celiac disease. New Eng. J. Med. 276: 996--1002. 4. Phillips, S. F., and W. H. J. Summerskill. 1966. Occlusion of the jejunum for intestinal perfusion in man. Proc. Mayo Clin. 41: 224-231. 5. Phillips, S. F., and W. H. J. Summerskill. 1966. Comparison of electrolyte transport in relation to intraluminal concentrations in the human jejunum and ileum (abstr.). J. Clin. Invest. 45: 1056. 6. Ewe, K., and W. H. J. Summerskill. 1965. Transfer of ammonia in the human jejunum. J. Lab. Clin. Med. 65: 839-847. 7. Smith. B. C. 1945. Experiences with the Miller-Abbott tube: a statistical study of 1,000 cases. Ann. Surg. 122: 253-259. 8. Berger, L., and S. Achs. 1947. Perforation of the small intestine by the Miller-Abbott tube. Surgery 22: 648-656.
Vol. 54, No.3
9. Bockus, H. L. 1964. Gastroenterology, Ed. 2, Vol. II, p. 67. W. B. Saunders Company, Philadelphia. 10. McGoon, D. C. 1956. Intussusception: a hazard of intestinal intubation. Surgery 40: 515-519. 11. Sower, N., and G. P. Wratten. 1965. Intussusception due to intestinal tubes: case reports and review of literature. Amer. J. Surg.ll0: 441-444. 12. Bloch, C., and H. M. Peck. 1964. Radiological notes: transient intussusception in sprue. J. Mount Sinai Hosp. N. Y. 31: 236-241. 13. Cortell, S., E. E. Rieber, T. W. Sheehy, and M. E. Conrad. 1967. Tropical sprue and intussusception: an unusual complication: report of a case. Amer. J. Dig. Dis. 12: 216-221. 14. Read, A. E., A. M. Dawson, D. N. S. Kerr, M. D. Turner, and S. Sherlock. 1960. Bleeding oesophageal varices treated by oesophageal compression tube. Brit. Med. J. 1: 227-231. 15. Garrett, J. M., W. H. J. Summerskill, and C. F. Code. 1966. Antral motility in patients with gastric ulcer. Amer. J. Dig. Dis. 11: 780-789. 16. Baker, D. R., W. H. Schrader, and C. R. Hitchcock. 1964. Small-bowel ulceration apparently associated with thiazide and potassium therapy. J. A. M. A.190: 586--590. 17. Lawrason, F. D., E. Alpert, F. L. Mohr, and F. G. McMahon. 1965. Ulcerative-obstructive lesions of the small intestine. J. A. M. A. 191: 641-644. 18. Warr, O. S., and J. P. Nash. 1967. Jejunal ulceration: report of a case apparently associated with potassium gluconate. J. A. M.A. 199: 217-218. 19. Phillips, S. F., and C. F. Code. 1966. Sorption of potassium in the small and large llltestine. Amer. J. Physiol. 211: 607-613.