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Stagnant loop syndrome resulting from small-bowel irradiation injury and intestinal by-pass
GYNECOLOGIC
ONCOLOGY
2,441-445
(1974)
Stagnant loop Syndrome Resulting Small-Bowel Irradiation Injury and Intestinal By-pass ROBERT Department
of Olxtetrics
W. SWAN
and Gynecology, William Beaumont El Paso, Texus 79920 Received
from
Army Medical
Center,
May 20,1974
Stagnant or blind-loop syndrome includes vitamin B12 malabsorption, steatorrhea, and bacterial overgrowth of the small intestine. A case is presented to demonstrate this syndrome occurring after small-bowel irradiation injury with exaggeration postenterocolic by-pass. Alteration of normal small-bowel flora is basic to development of the stagnantloop syndrome. Certain strains of bacteria as Bacteriodes and E. coli are capable of producing a malabsorption state. Definitive therapy for this syndrome developing after severe irradiation injury and intestinal by-pass includes antibiotics. Rapid symptomatic relief from diarrhea and improved malabsorption studies usually follow appropriate antibiotic therapy. Recolonization of the loop(s) with the offending bacterial species may produce exacerbation of symptoms. Since antibiotics are effective, recognition of this syndrome is important. Foul diarrhea1 stools should not be considered a necessary consequence of irradiation injury and intestinal by-pass.
Stagnant or blind-loop syndrome is a well-recognized clinical entity volving vitamin B12 malabsorption, steatorrhea, and bacterial overgrowth the small intestine [l-5]. Enterocolic bypass procedures are known to duce this syndrome [6-81. Not infrequently, a bypass may be necessary treatment of an intestinal irradiation injury where a partial obstruction malabsorption state already exist. The bypass may relieve obstructions compound the effects of the stagnant-loop syndrome. It is the purpose of this manuscript to make aware this relationship tween irradiation injury, intestinal bypass, and stagnant-loop syndrome. recent case will be presented relating these factors. The pathophysiology and treatment of stagnant-loop syndrome will be reviewed in the context intestinal irradiation injury and bypass. CASE B. N. is February dometriosis. During March 8,
inof profor and but beA of
PRESENTATION
a 50-yr-old Gl PI who had a stage-IIB 14, 1972. Two previous laparotomies surgery, thio-tepa 60 mg was 1972, external cobalt irradiation 441
Copyright @ 1974 by Academic Press, Inc. All rights of reproduction in any form reserved.
given was
ovarian cancer diagnosed on had been performed for enintravenously. initiated which
Beginning totaled 28
442
FIG. 1. Schematic
ROBERT
illustration
W.
SWAN
of severe irradiation
injury
to the small intestine
at laparotomy.
treatment days. Two thousand rads were delivered through 14 x 17-cm anterior and posterior pelvic portals with an additional 2800 rads delivered by the abdominal strip technique. Over an interval of 6 mo postirradiation, the patient developed signs and symptoms of intermittent partial obstruction and malabsorption. These included occasional vomiting, bloating, intermittent abdominal distention, cramping, malodorous diarrhea, 40-lb weight loss, and extreme fatigue. A large right lower-quadrant abdominopelvic mass developed which barium studies confirmed as containing several loops of small intestine. Multiple hospitalizations with intestinal intubation failed to improve her clinical course. On April 6, 1973, a fourth laparotomy was performed. Severe irradiation injury to the small intestine was confirmed (Fig. 1). All except 6 ft of proximal jejunum was involved in a compacted mass of dull, whitish, thick-
SMALL-BOWEL
IBBADIATION TABLE
443
INJURY
I
A COMPARISON OF LABORATORY DATA DURING VARIOUS PHASES OF TREATMENT PRE- AND POST-INTESTINAL BYPMS. Postbypass
Specimen
Normal value
Indican” (mgi24 hr) Fecal fat (g/24 hr) Schilling* (%/24 hr)
Urine Stool Urine
29-67 15 >12
D-XylOSe absorption (g/5 hr) Creatinine clearance (cclmin) Culture (pathogens)
Urine Urine Stool
>4 120 Negative
u Gross indication of intestinal tryptophan to indolic compounds creted in the urine. b IF = intrinsic factor.
bacterial activity which depends on the conversion of dietary by certain bacteria which are conjugated in the liver and ex-
Test
Prebypass 2.2
0.4 130 Negative
Preantibiotic 389 45 1.02 S IF 0.55 F IF 3.0 125 Negative
Postantibiotic 218; 172; 215 34 7 3.3 -
ened gut with multiple dilated loops. A side-to-side jejuno-ascending-enterocolostomy was performed. Although most symptoms abated immediately, the diarrhea1 stools worsened in frequency and odor especially with the use of antidiarrheal agents. Malabsorption studies were initiated with results supporting a stagnant-loop syndrome associated with bacterial overgrowth (Table I). Antibiotic therapy was initiated. Diarrhea subsided immediately but transiently on tetracycline. Neomycin and sulfadiazine were totally ineffective. A single course of clindamycin was followed by immediate resolution of diarrhea. Repeated malabsorption studies 1 mo after clindamycin therapy demonstrated an improved although not normal absorption pattern (Table I). Additional courses of clindamycin were necessary because of exacerbations of diarrhea. DISCUSSION This case is presented to illustrate the effects of an enterocolic bypass in a patient with a presumed preexisting stagnant-loop syndrome secondary to irradiation injury. Recognizing this relationship is important so as not to assume that any postoperative diarrhea is necessarily the result of “shortening” itself. The stagnant-loop syndrome involves a malabsorption state produced by alterations in the normal intestinal flora [l], Normally, there are no significar& coliform populations in the jejunum [1,4,9-111. However, the terminal ileum does contain significant numbers of coliforms, which resemble the fecal flora where obligate anaerobes as bacteroides [6,11,12], anaerobic lactobacilli [6,11], and enterobacteria [ 121 predominate [4]. Normal intestinal flora can be altered by reduced peristalsis in the small intestine [2,6,11,13,14]. Reducing effective peristalsis favors bacterial prolif-
444
ROBERT
W.
SWAN
eration and colonization [2,4,13], a condition which exists in chronically obstructed loops(s) of small intestine. If certain bacterial species colonize a stagnant loop, a malabsorption state can result [2,11,15]. Th is may include any combination of B12, fat, carbohydrate, and/or protein malabsorption [ 11. Stagnant loops frequently harbor a complex microflora [1,2,14,16]. Currently, certain species of Bacteroides [ 1,11,17] and coliforms [ 111 are considered offenders in producing malabsorption [ 111. E. coli can interfere with B12 absorption [15,18,19] w h’l1 e some Bacteroides species are known to deconjugate bile salts [4,17,20,21]. Either can utilize zylose and reduce zylose absorption [22]. Indicanuria can result from the metabolism of Bacteroides [6] and E. cob [6,19] species. E. coli [23,24], others have supAlthough some reports have implicated ported Bacteroides as being primarily responsible for malabsorption in the stagnant-loop syndrome [ 1,251. Bacteroides species represent the largest group of intestinal bacteria [1,12,20,26,27] and have been the most consistently cultured bacteria from stagnant loops [1,17,20,25,26]. In addition, they are typically sensitive to tetracycline [17] and lincomycin [17,25], the two most consistently successful antibiotics against bacterial overgrowth in the stagnant-loop syndrome. The present case demonstrates the salient features of stagnant loop syndrome [1,4,14]. They appeared in a patient whose presumed malabsorption postirradiation was exaggerated after a surgically created fistula and blind loop. Classic symptomatology including malaise, weight loss, malodorous diarrhea, and abdominal pain were present. Steatorrhea, B12 and zylose malabsorption had specific laboratory documentation. Finally, multiple dilated loops of gut containing stagnant intestinal fluid were present. Although not specifically documented, bacterial overgrowth in the small intestine was assumed based on significant indicanuria and prompt response of diarrhea to antibiotic therapy. Immediate response to tetracycline and clindamycin and the lack of effect from neomycin and sulfadiazine tend to support Bacteroides as the primary offending agent in this case. As intestinal by-pass procedures become more acceptable for the treatment of small-intestine irradiation injuries, stagnant-loop syndrome may become more of a problem in the future. Medical treatment should be directed toward eliminating the “pathologic bacteria” with appropriate antibiotic therapy. Hopefully, the loop(s) will be recolonized by “favorable bacteria” incapable of producing malabsorption. If complete elimination of responsible bacteria does not occur, malabsorption studies may not revert to normal. Despite the presence of stagnant loops and abnormal absorption studigs, patients can receive significant symptomatic relief, maintain weight, and live comfortably. REFERENCES 1. BROIDO, P. W., GORBACH, S. L., AND NYHUS, L. M. Microflora of the gastrointestinal tract and the surgical malabsorption syndromes, Surg. Gynecol. Obstet. 135, 449-460 (1972).
SMALL-BOWEL
IRRADIATION
INJURY
445
2. DONALDSON, R. M., JR. Role of enteric microorganisms in malabsorption, Fed. Proc. 26, 1426-1431 (1967). 3. DONALDSON, R. M., JR. Studies on the pathogenesis of steatorrhea in the blind-loop syndrome,J. Clin. lnoest. 44,1815-1825 (1965). 4. DONALDSON, R. M., JR. Small bowel bacterial overgrowth,Aduan. Intern. Med. 16, 191-212 (1970). 5. DONALDSON, R. M., JR. Normal bacterial populations of the intestine and their relation to intestinal function, N. Engl. J. Med. 270, 1050-1056 (1964). 6. TABAQCHALI, S., AND BOOTH, C. C. Relationship of the intestinal bacterial flora to absorption, Brit. Med. Bull. 23, 285-290 (1967). 7. CAMERON, D. G., WATSON, G. M., AND WITTS, L. J. The clinical association of macrocytic anemia with intestinal stricture and anastomosis, Blood 4, 793-802 (1949). 8. JEW, E. W., LEVOWITZ, B. S., AND FISHER, B. Alteration of the effects ofjejuno-colic fistula: an experimental study, Ann. Surg. 155,175-182 (1962). 9. GORBACH, S. L., PLAUT, A. G., NAHAS, L., AND WEINSTEIN, L. Studies of intestinal microflora II. Microorganisms of the small intestine and their relations to oral and fecal flora, Gastroenterology 53, 856-867 (1967). 10. HAMILTON, J. D., DYER, N. H., DAWSON, A. M., O’GRADY, F. W., VINCE, A., FENTON, J. C. B., AND MOLLIN, D. L. Assessment and significance of bacterial overgrowth in the small bowel, Quart, J. Med. 39,265-285 (1970). 11. GORBACH, S. L. Population control in the small bowel, Gut 8,530-532 (1967). 12. DONALDSON, R. M., JR. Normal bacterial populations of the intestine and their relation to intestinal function, N. Engl. J. Med. 270,938-945 (1964). 13. DIXON, J. M. S. The fate of bacteria in the small intestine, J. PuthoE. Bacterial. 79, 131-140 (1960). 14. DONALDSON, R. M., JR. Intestinal bacteria and malabsorption, Ann. Intern. Med. 64, 948-952 (1966). 15. PAULK, E. A., JR., AND FARRAR, W. E., JR. Diverticulosis of the small intestine and megaloblastic anemia, Amer. J. Med. 37,473-480 (1964). 16. DONALDSON, R. M., MCCONNELL, C., AND DEFFNER, N. Bacteriological studies in clinical and experimental blind-loop syndromes, Gastroenterology 52, 1082 (1967). 17. GORBACH, S. L., AND TABAQCHALI, S. Bacteria, bile, and the small bowel, Gut 10,963-972 (1969).
18. HALSTED, J. A., LEWIS, P. M., AND GASSTER, M. Absorption of radioactive vitamin B12 in the syndrome of megaloblastic anemia associated with intestinal stricture or anastomosis, Amer. J. Med. 20,42-52 (1956). 19. TABAQCHALI, S., OKUBADEJO, 0. A., NEALE, G., AND BOOTH, C. C. Influence of abnormal bacterial flora on small intestinal function, Proc. Roy. Sot. Med. 59, 1244-1246 (1966). 20. DRASAR, B. S., HILL, M. J., AND SHINER, M. The deconjugation of bile salts by human intestinal bacteria, Luncet 1, 1237-1238 (1966). 21. HILL, M. J., AND DRASAR, B. S. Degradation of bile salts by human intestinal bacteria, Gut 9,22-27 (1968). 22. GOLDSTEIN, F., CRIDEN, L. E., JENNER, E. R., AND WIRTS, C. W. Bacterial utilization of D-xylose, Gustroenterology 48,818-819 (1965). 23. TABAQCHALI, S., AND BOOTH, C. C. Jejunal bacteriology and bile-salt metabolism in patients with intestinal malabsorption, Lancet 2, 12-15 (1966). 24. PANISH, J. F. Experimental blind-loop steatorrhea, Gustroenterology 45, 394-399 (1963). 25. POLTER, D. E., BOYLE, J. D., MILLER, L. G., AND FINECOLD, S. M. Anaerobic bacteria as .; cause of the blind-loop syndrome, Gustroenterology 54, 1148-1154 (1968). 26. DRASAR, B. S., AND SHINER, M. Studies on the intestinal flora. II. Bacterial flora of the small intestine in patients with gastrointestinal disorders, Gut 10,812-819 (1969). 27. DRASAR, B. S., HUGHES, W. H., WILLIAMS, R. E. O., AND SHINER, M. Bacterial flora of the normal intestine, Proc. Roy. Sot. Med. 59, 1243 (1966).
ONCOLOGY
2,441-445
(1974)
Stagnant loop Syndrome Resulting Small-Bowel Irradiation Injury and Intestinal By-pass ROBERT Department
of Olxtetrics
W. SWAN
and Gynecology, William Beaumont El Paso, Texus 79920 Received
from
Army Medical
Center,
May 20,1974
Stagnant or blind-loop syndrome includes vitamin B12 malabsorption, steatorrhea, and bacterial overgrowth of the small intestine. A case is presented to demonstrate this syndrome occurring after small-bowel irradiation injury with exaggeration postenterocolic by-pass. Alteration of normal small-bowel flora is basic to development of the stagnantloop syndrome. Certain strains of bacteria as Bacteriodes and E. coli are capable of producing a malabsorption state. Definitive therapy for this syndrome developing after severe irradiation injury and intestinal by-pass includes antibiotics. Rapid symptomatic relief from diarrhea and improved malabsorption studies usually follow appropriate antibiotic therapy. Recolonization of the loop(s) with the offending bacterial species may produce exacerbation of symptoms. Since antibiotics are effective, recognition of this syndrome is important. Foul diarrhea1 stools should not be considered a necessary consequence of irradiation injury and intestinal by-pass.
Stagnant or blind-loop syndrome is a well-recognized clinical entity volving vitamin B12 malabsorption, steatorrhea, and bacterial overgrowth the small intestine [l-5]. Enterocolic bypass procedures are known to duce this syndrome [6-81. Not infrequently, a bypass may be necessary treatment of an intestinal irradiation injury where a partial obstruction malabsorption state already exist. The bypass may relieve obstructions compound the effects of the stagnant-loop syndrome. It is the purpose of this manuscript to make aware this relationship tween irradiation injury, intestinal bypass, and stagnant-loop syndrome. recent case will be presented relating these factors. The pathophysiology and treatment of stagnant-loop syndrome will be reviewed in the context intestinal irradiation injury and bypass. CASE B. N. is February dometriosis. During March 8,
inof profor and but beA of
PRESENTATION
a 50-yr-old Gl PI who had a stage-IIB 14, 1972. Two previous laparotomies surgery, thio-tepa 60 mg was 1972, external cobalt irradiation 441
Copyright @ 1974 by Academic Press, Inc. All rights of reproduction in any form reserved.
given was
ovarian cancer diagnosed on had been performed for enintravenously. initiated which
Beginning totaled 28
442
FIG. 1. Schematic
ROBERT
illustration
W.
SWAN
of severe irradiation
injury
to the small intestine
at laparotomy.
treatment days. Two thousand rads were delivered through 14 x 17-cm anterior and posterior pelvic portals with an additional 2800 rads delivered by the abdominal strip technique. Over an interval of 6 mo postirradiation, the patient developed signs and symptoms of intermittent partial obstruction and malabsorption. These included occasional vomiting, bloating, intermittent abdominal distention, cramping, malodorous diarrhea, 40-lb weight loss, and extreme fatigue. A large right lower-quadrant abdominopelvic mass developed which barium studies confirmed as containing several loops of small intestine. Multiple hospitalizations with intestinal intubation failed to improve her clinical course. On April 6, 1973, a fourth laparotomy was performed. Severe irradiation injury to the small intestine was confirmed (Fig. 1). All except 6 ft of proximal jejunum was involved in a compacted mass of dull, whitish, thick-
SMALL-BOWEL
IBBADIATION TABLE
443
INJURY
I
A COMPARISON OF LABORATORY DATA DURING VARIOUS PHASES OF TREATMENT PRE- AND POST-INTESTINAL BYPMS. Postbypass
Specimen
Normal value
Indican” (mgi24 hr) Fecal fat (g/24 hr) Schilling* (%/24 hr)
Urine Stool Urine
29-67 15 >12
D-XylOSe absorption (g/5 hr) Creatinine clearance (cclmin) Culture (pathogens)
Urine Urine Stool
>4 120 Negative
u Gross indication of intestinal tryptophan to indolic compounds creted in the urine. b IF = intrinsic factor.
bacterial activity which depends on the conversion of dietary by certain bacteria which are conjugated in the liver and ex-
Test
Prebypass 2.2
0.4 130 Negative
Preantibiotic 389 45 1.02 S IF 0.55 F IF 3.0 125 Negative
Postantibiotic 218; 172; 215 34 7 3.3 -
ened gut with multiple dilated loops. A side-to-side jejuno-ascending-enterocolostomy was performed. Although most symptoms abated immediately, the diarrhea1 stools worsened in frequency and odor especially with the use of antidiarrheal agents. Malabsorption studies were initiated with results supporting a stagnant-loop syndrome associated with bacterial overgrowth (Table I). Antibiotic therapy was initiated. Diarrhea subsided immediately but transiently on tetracycline. Neomycin and sulfadiazine were totally ineffective. A single course of clindamycin was followed by immediate resolution of diarrhea. Repeated malabsorption studies 1 mo after clindamycin therapy demonstrated an improved although not normal absorption pattern (Table I). Additional courses of clindamycin were necessary because of exacerbations of diarrhea. DISCUSSION This case is presented to illustrate the effects of an enterocolic bypass in a patient with a presumed preexisting stagnant-loop syndrome secondary to irradiation injury. Recognizing this relationship is important so as not to assume that any postoperative diarrhea is necessarily the result of “shortening” itself. The stagnant-loop syndrome involves a malabsorption state produced by alterations in the normal intestinal flora [l], Normally, there are no significar& coliform populations in the jejunum [1,4,9-111. However, the terminal ileum does contain significant numbers of coliforms, which resemble the fecal flora where obligate anaerobes as bacteroides [6,11,12], anaerobic lactobacilli [6,11], and enterobacteria [ 121 predominate [4]. Normal intestinal flora can be altered by reduced peristalsis in the small intestine [2,6,11,13,14]. Reducing effective peristalsis favors bacterial prolif-
444
ROBERT
W.
SWAN
eration and colonization [2,4,13], a condition which exists in chronically obstructed loops(s) of small intestine. If certain bacterial species colonize a stagnant loop, a malabsorption state can result [2,11,15]. Th is may include any combination of B12, fat, carbohydrate, and/or protein malabsorption [ 11. Stagnant loops frequently harbor a complex microflora [1,2,14,16]. Currently, certain species of Bacteroides [ 1,11,17] and coliforms [ 111 are considered offenders in producing malabsorption [ 111. E. coli can interfere with B12 absorption [15,18,19] w h’l1 e some Bacteroides species are known to deconjugate bile salts [4,17,20,21]. Either can utilize zylose and reduce zylose absorption [22]. Indicanuria can result from the metabolism of Bacteroides [6] and E. cob [6,19] species. E. coli [23,24], others have supAlthough some reports have implicated ported Bacteroides as being primarily responsible for malabsorption in the stagnant-loop syndrome [ 1,251. Bacteroides species represent the largest group of intestinal bacteria [1,12,20,26,27] and have been the most consistently cultured bacteria from stagnant loops [1,17,20,25,26]. In addition, they are typically sensitive to tetracycline [17] and lincomycin [17,25], the two most consistently successful antibiotics against bacterial overgrowth in the stagnant-loop syndrome. The present case demonstrates the salient features of stagnant loop syndrome [1,4,14]. They appeared in a patient whose presumed malabsorption postirradiation was exaggerated after a surgically created fistula and blind loop. Classic symptomatology including malaise, weight loss, malodorous diarrhea, and abdominal pain were present. Steatorrhea, B12 and zylose malabsorption had specific laboratory documentation. Finally, multiple dilated loops of gut containing stagnant intestinal fluid were present. Although not specifically documented, bacterial overgrowth in the small intestine was assumed based on significant indicanuria and prompt response of diarrhea to antibiotic therapy. Immediate response to tetracycline and clindamycin and the lack of effect from neomycin and sulfadiazine tend to support Bacteroides as the primary offending agent in this case. As intestinal by-pass procedures become more acceptable for the treatment of small-intestine irradiation injuries, stagnant-loop syndrome may become more of a problem in the future. Medical treatment should be directed toward eliminating the “pathologic bacteria” with appropriate antibiotic therapy. Hopefully, the loop(s) will be recolonized by “favorable bacteria” incapable of producing malabsorption. If complete elimination of responsible bacteria does not occur, malabsorption studies may not revert to normal. Despite the presence of stagnant loops and abnormal absorption studigs, patients can receive significant symptomatic relief, maintain weight, and live comfortably. REFERENCES 1. BROIDO, P. W., GORBACH, S. L., AND NYHUS, L. M. Microflora of the gastrointestinal tract and the surgical malabsorption syndromes, Surg. Gynecol. Obstet. 135, 449-460 (1972).
SMALL-BOWEL
IRRADIATION
INJURY
445
2. DONALDSON, R. M., JR. Role of enteric microorganisms in malabsorption, Fed. Proc. 26, 1426-1431 (1967). 3. DONALDSON, R. M., JR. Studies on the pathogenesis of steatorrhea in the blind-loop syndrome,J. Clin. lnoest. 44,1815-1825 (1965). 4. DONALDSON, R. M., JR. Small bowel bacterial overgrowth,Aduan. Intern. Med. 16, 191-212 (1970). 5. DONALDSON, R. M., JR. Normal bacterial populations of the intestine and their relation to intestinal function, N. Engl. J. Med. 270, 1050-1056 (1964). 6. TABAQCHALI, S., AND BOOTH, C. C. Relationship of the intestinal bacterial flora to absorption, Brit. Med. Bull. 23, 285-290 (1967). 7. CAMERON, D. G., WATSON, G. M., AND WITTS, L. J. The clinical association of macrocytic anemia with intestinal stricture and anastomosis, Blood 4, 793-802 (1949). 8. JEW, E. W., LEVOWITZ, B. S., AND FISHER, B. Alteration of the effects ofjejuno-colic fistula: an experimental study, Ann. Surg. 155,175-182 (1962). 9. GORBACH, S. L., PLAUT, A. G., NAHAS, L., AND WEINSTEIN, L. Studies of intestinal microflora II. Microorganisms of the small intestine and their relations to oral and fecal flora, Gastroenterology 53, 856-867 (1967). 10. HAMILTON, J. D., DYER, N. H., DAWSON, A. M., O’GRADY, F. W., VINCE, A., FENTON, J. C. B., AND MOLLIN, D. L. Assessment and significance of bacterial overgrowth in the small bowel, Quart, J. Med. 39,265-285 (1970). 11. GORBACH, S. L. Population control in the small bowel, Gut 8,530-532 (1967). 12. DONALDSON, R. M., JR. Normal bacterial populations of the intestine and their relation to intestinal function, N. Engl. J. Med. 270,938-945 (1964). 13. DIXON, J. M. S. The fate of bacteria in the small intestine, J. PuthoE. Bacterial. 79, 131-140 (1960). 14. DONALDSON, R. M., JR. Intestinal bacteria and malabsorption, Ann. Intern. Med. 64, 948-952 (1966). 15. PAULK, E. A., JR., AND FARRAR, W. E., JR. Diverticulosis of the small intestine and megaloblastic anemia, Amer. J. Med. 37,473-480 (1964). 16. DONALDSON, R. M., MCCONNELL, C., AND DEFFNER, N. Bacteriological studies in clinical and experimental blind-loop syndromes, Gastroenterology 52, 1082 (1967). 17. GORBACH, S. L., AND TABAQCHALI, S. Bacteria, bile, and the small bowel, Gut 10,963-972 (1969).
18. HALSTED, J. A., LEWIS, P. M., AND GASSTER, M. Absorption of radioactive vitamin B12 in the syndrome of megaloblastic anemia associated with intestinal stricture or anastomosis, Amer. J. Med. 20,42-52 (1956). 19. TABAQCHALI, S., OKUBADEJO, 0. A., NEALE, G., AND BOOTH, C. C. Influence of abnormal bacterial flora on small intestinal function, Proc. Roy. Sot. Med. 59, 1244-1246 (1966). 20. DRASAR, B. S., HILL, M. J., AND SHINER, M. The deconjugation of bile salts by human intestinal bacteria, Luncet 1, 1237-1238 (1966). 21. HILL, M. J., AND DRASAR, B. S. Degradation of bile salts by human intestinal bacteria, Gut 9,22-27 (1968). 22. GOLDSTEIN, F., CRIDEN, L. E., JENNER, E. R., AND WIRTS, C. W. Bacterial utilization of D-xylose, Gustroenterology 48,818-819 (1965). 23. TABAQCHALI, S., AND BOOTH, C. C. Jejunal bacteriology and bile-salt metabolism in patients with intestinal malabsorption, Lancet 2, 12-15 (1966). 24. PANISH, J. F. Experimental blind-loop steatorrhea, Gustroenterology 45, 394-399 (1963). 25. POLTER, D. E., BOYLE, J. D., MILLER, L. G., AND FINECOLD, S. M. Anaerobic bacteria as .; cause of the blind-loop syndrome, Gustroenterology 54, 1148-1154 (1968). 26. DRASAR, B. S., AND SHINER, M. Studies on the intestinal flora. II. Bacterial flora of the small intestine in patients with gastrointestinal disorders, Gut 10,812-819 (1969). 27. DRASAR, B. S., HUGHES, W. H., WILLIAMS, R. E. O., AND SHINER, M. Bacterial flora of the normal intestine, Proc. Roy. Sot. Med. 59, 1243 (1966).