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Detection of Enteric-Urinary Fistulas with a Noninvasive Quantitative Method
0022-534 7/84/1326-1134$02.00 /0
Vol. 132, December Printed in U.S.A.
THE JOURNAL OF UROLOGY
Copyright© 1984 by The Williams & Wilkins Co.
DETECTION OF ENTERIC-URINARY FISTULAS WITH A NONINVASIVE QUANTITATIVE METHOD MARGUERITE C. LIPPERT,* CHARLES D. TEATES AND STUART S. HOWARDS From the Departments of Urology and Radiology, University of Virginia Hospital, Charlottesville, Virginia
ABSTRACT
The 51 chromium test is an inexpensive, noninvasive test to evaluate patients for enteric-urinary fistulas. Of 11 patients studied the 51 chromium test demonstrated correctly a fistula in 5 of 6 patients with fistulas and showed no lesion in all 5 without fistulas. Excretory urography, barium enemas, visible contrast medium, cystograms and upper gastrointestinal series failed to demonstrate the fistulas with similar accuracy. Cystoscopy suggested a possible lesion in 4 patients but was definite for a fistula in only 2 of those patients. A vesicoenteric fistula occurs in only 1 of 3,000 surgical hospitalizations. 1 Characteristic symptoms of pneumaturia, dysuria and fecaluria, and a history of recurrent urinary tract infections have been known to suggest a urinary-enteric fistula. However, it often is difficult to document the presence of a fistula despite the availability of many recognized tests, such as excretory urography (IVP), cystography, barium enema, cystoscopy and proctoscopy, and the use of visible contrast medium, such as charcoal or pyrvinium pamoate. Since little 51 chromium (51 Cr)-labeled sodium chromate is absorbed from the gastrointestinal tract the presence of a significant quantity of 51 Cr in the urine after ingestion of the isotope suggests a urinary-enteric fistula. When 51 Cr sodium chromate was given orally to a normal subject <0.5 per cent of the radioactive sodium chromate bound to red cells was excreted in the urine. After 2 subjects ingested free 51 Cr in grape juice 96.3 and 92.8 per cent of the compound, respectively, were recovered in a 5-day fecal collection. 2 When 8 patients ingested 51 Cr-labeled albumin no radioactivity was detectable in the urine. 3 Twelve patients ingested 51 Cr-labeled albumin and 93 to 99 per cent of the 51 Cr was excreted in the stools during the next 10 days. 4 Unlike urinary charcoal 51 Cr in the urine can be quantitated over time, allowing for more objective analysis. These facts provided the rationale for development of a new test to screen patients for the presence of a urinary-enteric fistula. We review our experience with this test. MATERIALS AND METHODS
We reviewed the records of 11 patients who were evaluated for enteric-urinary fistulas with the 51 Cr test from 1978 to 1981. These patients also were evaluated with roentgenologic studies, including IVPs, barium enemas, cystograms, upper gastrointestinal series and/or retrograde ureterograms. Other diagnostic modalities included proctosigmoidoscopy, cystoscopy, orally administered visible contrast medium, such as charcoal and pyrvinium pamoate, and/or surgical exploration. The 8 men and 3 women ranged from 28 to 71 years old (mean 55 years). All patients underwent the 51 Cr test. The patients ingested 30 µCi. 51 Cr-labeled sodium chromate diluted in 30 cc water. Urine was collected for 48 to 72 hours (8-hour aliquots for the first 24 hours and then as 24-hour urinary specimens for 2 days). The volumes were recorded and 3 cc samples of each aliquot were counted at the end of the study in a standard gamma counter, allowing calculation of the cumulative percentage 51 Cr excreted in the urine. Urine was voided except for
Accepted for publication March 2, 1984.
* Requests for reprints: Department of Urology, Box 422, University of Virginia School of Medicine, Charlottesville, Virginia 22908.
1 patient whose urine was collected with ureteral catheters. All patients were alert and cooperative so that stool contamination was avoided by instructing the women to clean the genital area with soap and water before voiding and the men to use a urinal when voiding. RESULTS
After extensive evaluation 6 patients had a proved entericurinary fistula and 5 did not. The 51 Cr test demonstrated a fistula in 5 of 6 patients with fistulas and failed to demonstrate a fistula in all 5 without a fistula. Presenting complaints of patients and the other diagnostic tests failed to differentiate the 2 groups as well. Presenting complaints of patients revealed an almost equal incidence of recurrent urinary tract infections, pneumaturia and dysuria in patients with and without fistulas (table 1). Patients were evaluated for enteric-urinary fistulas because of symptoms and history characteristically suggestive of a fistula. The pneumaturia in 4 patients without a fistula was believed, in retrospect, to be secondary to imprecise history taking in 2, gas-forming bacteria in 1 poorly controlled diabetic and unexplained causes in 1. Of the various diagnostic tests used the 51 Cr test diagnosed the enteric-urinary fistulas most accurately (table 2). IVP, cystography and upper gastrointestinal series failed to show any fistulas. Cystoscopy demonstrated a probable fistula in 2 patients (33 per cent), an erythematous lesion in 1 (16.5 per cent) and an ulcer in 1 (16.5 per cent). The oral 51Cr test demonstrated fistulas correctly in 5 of 6 patients (83 per cent), including 1 (25 per cent) in whom the oral charcoal test was positive, 2 in whom the charcoal test was negative for a fistula and 1 in whom the pyrvinium pamoate test failed to demonstrate a fistula. The 51 Cr test demonstrated that 5 of 6 patients with a fistula excreted 0.66 to 1.8 per cent of the ingested dose within 48 hours, whereas 5 without a fistula excreted 0.08 to 0.58 per cent of the dose within 48 hours (see figure). In 1 patient with bilateral ureteral catheters the excretion of 51 Cr from the right ureter was >2 times the excretion from the left ureter, which allowed localization of the fistula. Of the 6 patients with fistulas 5 were confirmed at operation and 1 by a fistulogram during proctoscopy. Of the 5 patients without fistulas the absence of a fistula was confirmed in 1 by 2 surgical explorations, while 4 had thorough but completely negative cystoscopic and radiologic evaluations and were found to have another etiology for the recurrent urinary tract infections. In the 6 patients with fistulas the etiology was colon carcinoma in 2 men, diverticulosis in 1 woman, Crohn's disease in 1 man, Hirschsprung's disease with scar tissue from previous
1134
DETECTI01\J OF EN'1'ERIC-URIN1-\,J:~Y F .!.~TULA0 ~llITH NOI\JINVASIVE QUP-J~~-·'TI'l'ATIVE fvlETJ:-IOD
surgical procedures in 1 man and scar pv,o~c,vq from a of these previous Billroth I nnwa,c11·,ro in l man. patients (except the patient with known Hirschsprung's disease) presented with recurrent urinary tract infections only. Therefore, the etiology of the fistula was not known until the patients underwent evaluation for a fistula. In the patients without fistulas the etiology of the recurrent urinary tract infections was chronic bacterial prostatitis in 3 men, poorly controlled diabetes in 1 woman and natural susceptibility to recurrent urinary tract infections in 1 woman. These patients also presented primarily for evaluation of recurrent urinary tract infections. Additionally, 1 woman had known diabetes and 1 had known diverticulosis. Therefore, both groups were similar in presentation. The patient in whom the 51 Cr test failed to reveal a fistula correctly presented with episodes of pneumaturia and recurrent urinary tract infections accompanied by malaise. He also had a negative barium enema, upper gastrointestinal series, oral charcoal test, cystogram, cystoscopy and IVP. However, all of these studies (including the 51 Cr test) were done between episodes when he had no pneumaturia, infection or malaise. The fistula was found during an operation to correct a possible small bowel hernia seen on the upper gastrointestinal series. The TABLE 1.
Presenting complaints of evaluated patients Pts. With Fistulas
Pts. Without Fistulas
6
5 5
No. pts. Recurrent urinary tract infections Pneumaturia Dysuria Fecaluria Urine per rectum
TABLE 2.
6 4
4 4 0 0
5
1 0
Diagnostic tests
Pts. With Fistula (No. pos./No. tested)
IVP
Pts. Without Fistula (No. tested)* 5 5 2 3 3
0/6 2/6
Cystoscopy Cystogram Barium enema Upper gastrointestinal series Retrograde ureterography Proctoscopy Oral charcoal Pyrvinium pamoate
0/4t 1/5 0/2
0/2 1/1 1/4 0/1 5/6
51Cr
1 0
1 0 5
* All patients tested had negahve results. -t Two other patients had a suspicious test although fistulas were not demonstrated conclusively.
also had to the In retrospect, this fistula and closed intermittently with exacerbations of causing malaise, pneumaturia and urinary tract infections. Unfortunately, the entire fistula evaluation was done when he was without symptoms and, possibly, without an open fistula. DISCUSSION
The diagnosis of enteric-urinary fistulas can be complex, costly and, occasionally, difficult. Shield and associates found that IVPs and cystography rarely are helpful in establishing the presence of a fistula in cases of inflammatory bowel disease. 5 Cystoscopy was found to be the most sensitive method of diagnosis in vesicoenteric fistulas but more often revealed only suggestive evidence, such as erythema, cystitis, edema or localized inflammation, rather than a fistula. 6 Krompier and associates believed cystoscopy to be the most helpful test for diagnosis of vesicocolonic fistulas. 7 However, they were able to diagnose 4 of 4 patients with visible contrast medium even when radiographic methods failed in 2. Ward and associates suggested that orally administered charcoal was useful in obtaining confirmatory evidence of a colovesical fistula, since it should be seen in the urine as black particles. 8 Morse and Dretler found that the "most productive, easiest, and least expensive" method to diagnose a colovesical fistula is to start with oral contrast medium. 9 They were able to diagnose 4 of 5 colovesical fistulas with visible contrast medium and believed that further radiographic tests were merely to localize the fistula. The 51 Cr test also is inexpensive and noninvasive, and can be done as an outpatient procedure. 51 Cr-labeled sodium chromate is nontoxic orally, not absorbed in the bowe1, 2- 4 not adsorbed to bowel contents or mucosa and has a long shelf life. In addition, it can be quantitated readily in the urine while charcoal cannot be quantitated routinely. Furthermore, localization can be accomplished to some degree with split urinary collections with ureteral catheters. Although 51 Cr is an optimal tracer to diagnose a minary-enteric fistula because it is not absorbed by the bowel, is small enough to pass through a fistula and can be detected easily in the urine, it cannot give a high resolution image, as can 198gold coiloid. 10 Therefore, in our study a fistula is diagnosed by the presence of a significant amount of 51 Cr in the urine and not by a visual image. Of all the diagnostic studies used we found that the 51 Cr test diagnosed enteric-urinary fistulas most correctly (5 of 6 paCystoscopy was diagnostic in 2 of 6 µaic1e,n::; and was somewhat suggestive in 2 more ,-.-v,-,.,v,v. test had a false """'"·''v'" result, including the 51 Cr test. nere1or1~, the 51 Cr
20~ Patients with no fislulae
C:
0 +-
Patient wilh a fistula nol demonstrated on chromium 51 lest
~ u ,<
w
c
1.0
(I)
u ,_
Q_
0.6
----- _..--- -----
0.4 0.2
~?'- - - - - --~::.::..::.:::.::.::.::-.=::::..-::..........::.-:.::·:.:·=·::.::;·.::.-:::·.:.::::.:. 12
24
36
1135
48
60
72
Hours of Urine Collection Excretion of 51 Cr in urine of patients with and without fistulas
1136
LIPPERT, TEATES AND HOWARDS
test is a cost-effective, reliable screening procedure for patients with enteric-urinary fistulas. REFERENCES 1. Pugh, J. I.: On the pathology and behaviour of acquired nontraumatic vesico-intestinal fistula. Brit. J. Surg., 51: 644, 1964. 2. Eubaugh, F. G., Jr., Clemens, T., Jr., Rodnan, G. and Peterson, R. E.: Quantitative measurement of gastrointestinal blood loss. 1. The use of radioactive Cr51 in patients with gastrointestinal bleeding. Amer. J. Med., 25: 169, 1958. 3. Waldmann, T. A.: Gastrointestinal protein loss demonstrated by Cr51 -labelled albumin. Lancet, 2: 121, 1961. 4. Waldmann, T. A., Wochner, R. D. and Strober, W.: The role of gastrointestinal tract in plasma protein metabolism. Studies with 51Cr-albumin. Amer. J. Med., 46: 275, 1969.
5. Shield, D. E., Lytton, B., Weiss, R. M. and Schiff, M., Jr.: Urologic complications of inflammatory bowel disease. J. Urol., 115: 701, 1976. 6. Carson, C. C., Malek, R. S. and Remine, W. H.: Urologic aspects of vesicoenteric fistulas. J. Urol., 119: 744, 1978. 7. Krompier, A., Howard, R., MacEwen, A., Natoli, C. and Wear, J. B.: Vesicocolonic fistulas in diverticulitis. J. Urol., 115: 664, 1976. 8. Ward, J. N., Lavengood, R. W., Jr., Nay, H. R. and Draper, J. W.: Diagnosis and treatment of colovesical fistulas. Surg., Gynec. & Obst., 130: 1082, 1970. 9. Morse, F. P., III and Dretler, S. P.: Diagnosis and treatment of colovesical fistula. J. Urol., 111: 22, 1974. 10. Prokop, E. K., Buddemeyer, E. U., Strauss, H. W. and Wagner, H. N., Jr.: Detection and localization of an occult vesicoenteric fistula. Amer. J. Roentgen., 121: 811, 1974.
Vol. 132, December Printed in U.S.A.
THE JOURNAL OF UROLOGY
Copyright© 1984 by The Williams & Wilkins Co.
DETECTION OF ENTERIC-URINARY FISTULAS WITH A NONINVASIVE QUANTITATIVE METHOD MARGUERITE C. LIPPERT,* CHARLES D. TEATES AND STUART S. HOWARDS From the Departments of Urology and Radiology, University of Virginia Hospital, Charlottesville, Virginia
ABSTRACT
The 51 chromium test is an inexpensive, noninvasive test to evaluate patients for enteric-urinary fistulas. Of 11 patients studied the 51 chromium test demonstrated correctly a fistula in 5 of 6 patients with fistulas and showed no lesion in all 5 without fistulas. Excretory urography, barium enemas, visible contrast medium, cystograms and upper gastrointestinal series failed to demonstrate the fistulas with similar accuracy. Cystoscopy suggested a possible lesion in 4 patients but was definite for a fistula in only 2 of those patients. A vesicoenteric fistula occurs in only 1 of 3,000 surgical hospitalizations. 1 Characteristic symptoms of pneumaturia, dysuria and fecaluria, and a history of recurrent urinary tract infections have been known to suggest a urinary-enteric fistula. However, it often is difficult to document the presence of a fistula despite the availability of many recognized tests, such as excretory urography (IVP), cystography, barium enema, cystoscopy and proctoscopy, and the use of visible contrast medium, such as charcoal or pyrvinium pamoate. Since little 51 chromium (51 Cr)-labeled sodium chromate is absorbed from the gastrointestinal tract the presence of a significant quantity of 51 Cr in the urine after ingestion of the isotope suggests a urinary-enteric fistula. When 51 Cr sodium chromate was given orally to a normal subject <0.5 per cent of the radioactive sodium chromate bound to red cells was excreted in the urine. After 2 subjects ingested free 51 Cr in grape juice 96.3 and 92.8 per cent of the compound, respectively, were recovered in a 5-day fecal collection. 2 When 8 patients ingested 51 Cr-labeled albumin no radioactivity was detectable in the urine. 3 Twelve patients ingested 51 Cr-labeled albumin and 93 to 99 per cent of the 51 Cr was excreted in the stools during the next 10 days. 4 Unlike urinary charcoal 51 Cr in the urine can be quantitated over time, allowing for more objective analysis. These facts provided the rationale for development of a new test to screen patients for the presence of a urinary-enteric fistula. We review our experience with this test. MATERIALS AND METHODS
We reviewed the records of 11 patients who were evaluated for enteric-urinary fistulas with the 51 Cr test from 1978 to 1981. These patients also were evaluated with roentgenologic studies, including IVPs, barium enemas, cystograms, upper gastrointestinal series and/or retrograde ureterograms. Other diagnostic modalities included proctosigmoidoscopy, cystoscopy, orally administered visible contrast medium, such as charcoal and pyrvinium pamoate, and/or surgical exploration. The 8 men and 3 women ranged from 28 to 71 years old (mean 55 years). All patients underwent the 51 Cr test. The patients ingested 30 µCi. 51 Cr-labeled sodium chromate diluted in 30 cc water. Urine was collected for 48 to 72 hours (8-hour aliquots for the first 24 hours and then as 24-hour urinary specimens for 2 days). The volumes were recorded and 3 cc samples of each aliquot were counted at the end of the study in a standard gamma counter, allowing calculation of the cumulative percentage 51 Cr excreted in the urine. Urine was voided except for
Accepted for publication March 2, 1984.
* Requests for reprints: Department of Urology, Box 422, University of Virginia School of Medicine, Charlottesville, Virginia 22908.
1 patient whose urine was collected with ureteral catheters. All patients were alert and cooperative so that stool contamination was avoided by instructing the women to clean the genital area with soap and water before voiding and the men to use a urinal when voiding. RESULTS
After extensive evaluation 6 patients had a proved entericurinary fistula and 5 did not. The 51 Cr test demonstrated a fistula in 5 of 6 patients with fistulas and failed to demonstrate a fistula in all 5 without a fistula. Presenting complaints of patients and the other diagnostic tests failed to differentiate the 2 groups as well. Presenting complaints of patients revealed an almost equal incidence of recurrent urinary tract infections, pneumaturia and dysuria in patients with and without fistulas (table 1). Patients were evaluated for enteric-urinary fistulas because of symptoms and history characteristically suggestive of a fistula. The pneumaturia in 4 patients without a fistula was believed, in retrospect, to be secondary to imprecise history taking in 2, gas-forming bacteria in 1 poorly controlled diabetic and unexplained causes in 1. Of the various diagnostic tests used the 51 Cr test diagnosed the enteric-urinary fistulas most accurately (table 2). IVP, cystography and upper gastrointestinal series failed to show any fistulas. Cystoscopy demonstrated a probable fistula in 2 patients (33 per cent), an erythematous lesion in 1 (16.5 per cent) and an ulcer in 1 (16.5 per cent). The oral 51Cr test demonstrated fistulas correctly in 5 of 6 patients (83 per cent), including 1 (25 per cent) in whom the oral charcoal test was positive, 2 in whom the charcoal test was negative for a fistula and 1 in whom the pyrvinium pamoate test failed to demonstrate a fistula. The 51 Cr test demonstrated that 5 of 6 patients with a fistula excreted 0.66 to 1.8 per cent of the ingested dose within 48 hours, whereas 5 without a fistula excreted 0.08 to 0.58 per cent of the dose within 48 hours (see figure). In 1 patient with bilateral ureteral catheters the excretion of 51 Cr from the right ureter was >2 times the excretion from the left ureter, which allowed localization of the fistula. Of the 6 patients with fistulas 5 were confirmed at operation and 1 by a fistulogram during proctoscopy. Of the 5 patients without fistulas the absence of a fistula was confirmed in 1 by 2 surgical explorations, while 4 had thorough but completely negative cystoscopic and radiologic evaluations and were found to have another etiology for the recurrent urinary tract infections. In the 6 patients with fistulas the etiology was colon carcinoma in 2 men, diverticulosis in 1 woman, Crohn's disease in 1 man, Hirschsprung's disease with scar tissue from previous
1134
DETECTI01\J OF EN'1'ERIC-URIN1-\,J:~Y F .!.~TULA0 ~llITH NOI\JINVASIVE QUP-J~~-·'TI'l'ATIVE fvlETJ:-IOD
surgical procedures in 1 man and scar pv,o~c,vq from a of these previous Billroth I nnwa,c11·,ro in l man. patients (except the patient with known Hirschsprung's disease) presented with recurrent urinary tract infections only. Therefore, the etiology of the fistula was not known until the patients underwent evaluation for a fistula. In the patients without fistulas the etiology of the recurrent urinary tract infections was chronic bacterial prostatitis in 3 men, poorly controlled diabetes in 1 woman and natural susceptibility to recurrent urinary tract infections in 1 woman. These patients also presented primarily for evaluation of recurrent urinary tract infections. Additionally, 1 woman had known diabetes and 1 had known diverticulosis. Therefore, both groups were similar in presentation. The patient in whom the 51 Cr test failed to reveal a fistula correctly presented with episodes of pneumaturia and recurrent urinary tract infections accompanied by malaise. He also had a negative barium enema, upper gastrointestinal series, oral charcoal test, cystogram, cystoscopy and IVP. However, all of these studies (including the 51 Cr test) were done between episodes when he had no pneumaturia, infection or malaise. The fistula was found during an operation to correct a possible small bowel hernia seen on the upper gastrointestinal series. The TABLE 1.
Presenting complaints of evaluated patients Pts. With Fistulas
Pts. Without Fistulas
6
5 5
No. pts. Recurrent urinary tract infections Pneumaturia Dysuria Fecaluria Urine per rectum
TABLE 2.
6 4
4 4 0 0
5
1 0
Diagnostic tests
Pts. With Fistula (No. pos./No. tested)
IVP
Pts. Without Fistula (No. tested)* 5 5 2 3 3
0/6 2/6
Cystoscopy Cystogram Barium enema Upper gastrointestinal series Retrograde ureterography Proctoscopy Oral charcoal Pyrvinium pamoate
0/4t 1/5 0/2
0/2 1/1 1/4 0/1 5/6
51Cr
1 0
1 0 5
* All patients tested had negahve results. -t Two other patients had a suspicious test although fistulas were not demonstrated conclusively.
also had to the In retrospect, this fistula and closed intermittently with exacerbations of causing malaise, pneumaturia and urinary tract infections. Unfortunately, the entire fistula evaluation was done when he was without symptoms and, possibly, without an open fistula. DISCUSSION
The diagnosis of enteric-urinary fistulas can be complex, costly and, occasionally, difficult. Shield and associates found that IVPs and cystography rarely are helpful in establishing the presence of a fistula in cases of inflammatory bowel disease. 5 Cystoscopy was found to be the most sensitive method of diagnosis in vesicoenteric fistulas but more often revealed only suggestive evidence, such as erythema, cystitis, edema or localized inflammation, rather than a fistula. 6 Krompier and associates believed cystoscopy to be the most helpful test for diagnosis of vesicocolonic fistulas. 7 However, they were able to diagnose 4 of 4 patients with visible contrast medium even when radiographic methods failed in 2. Ward and associates suggested that orally administered charcoal was useful in obtaining confirmatory evidence of a colovesical fistula, since it should be seen in the urine as black particles. 8 Morse and Dretler found that the "most productive, easiest, and least expensive" method to diagnose a colovesical fistula is to start with oral contrast medium. 9 They were able to diagnose 4 of 5 colovesical fistulas with visible contrast medium and believed that further radiographic tests were merely to localize the fistula. The 51 Cr test also is inexpensive and noninvasive, and can be done as an outpatient procedure. 51 Cr-labeled sodium chromate is nontoxic orally, not absorbed in the bowe1, 2- 4 not adsorbed to bowel contents or mucosa and has a long shelf life. In addition, it can be quantitated readily in the urine while charcoal cannot be quantitated routinely. Furthermore, localization can be accomplished to some degree with split urinary collections with ureteral catheters. Although 51 Cr is an optimal tracer to diagnose a minary-enteric fistula because it is not absorbed by the bowel, is small enough to pass through a fistula and can be detected easily in the urine, it cannot give a high resolution image, as can 198gold coiloid. 10 Therefore, in our study a fistula is diagnosed by the presence of a significant amount of 51 Cr in the urine and not by a visual image. Of all the diagnostic studies used we found that the 51 Cr test diagnosed enteric-urinary fistulas most correctly (5 of 6 paCystoscopy was diagnostic in 2 of 6 µaic1e,n::; and was somewhat suggestive in 2 more ,-.-v,-,.,v,v. test had a false """'"·''v'" result, including the 51 Cr test. nere1or1~, the 51 Cr
20~ Patients with no fislulae
C:
0 +-
Patient wilh a fistula nol demonstrated on chromium 51 lest
~ u ,<
w
c
1.0
(I)
u ,_
Q_
0.6
----- _..--- -----
0.4 0.2
~?'- - - - - --~::.::..::.:::.::.::.::-.=::::..-::..........::.-:.::·:.:·=·::.::;·.::.-:::·.:.::::.:. 12
24
36
1135
48
60
72
Hours of Urine Collection Excretion of 51 Cr in urine of patients with and without fistulas
1136
LIPPERT, TEATES AND HOWARDS
test is a cost-effective, reliable screening procedure for patients with enteric-urinary fistulas. REFERENCES 1. Pugh, J. I.: On the pathology and behaviour of acquired nontraumatic vesico-intestinal fistula. Brit. J. Surg., 51: 644, 1964. 2. Eubaugh, F. G., Jr., Clemens, T., Jr., Rodnan, G. and Peterson, R. E.: Quantitative measurement of gastrointestinal blood loss. 1. The use of radioactive Cr51 in patients with gastrointestinal bleeding. Amer. J. Med., 25: 169, 1958. 3. Waldmann, T. A.: Gastrointestinal protein loss demonstrated by Cr51 -labelled albumin. Lancet, 2: 121, 1961. 4. Waldmann, T. A., Wochner, R. D. and Strober, W.: The role of gastrointestinal tract in plasma protein metabolism. Studies with 51Cr-albumin. Amer. J. Med., 46: 275, 1969.
5. Shield, D. E., Lytton, B., Weiss, R. M. and Schiff, M., Jr.: Urologic complications of inflammatory bowel disease. J. Urol., 115: 701, 1976. 6. Carson, C. C., Malek, R. S. and Remine, W. H.: Urologic aspects of vesicoenteric fistulas. J. Urol., 119: 744, 1978. 7. Krompier, A., Howard, R., MacEwen, A., Natoli, C. and Wear, J. B.: Vesicocolonic fistulas in diverticulitis. J. Urol., 115: 664, 1976. 8. Ward, J. N., Lavengood, R. W., Jr., Nay, H. R. and Draper, J. W.: Diagnosis and treatment of colovesical fistulas. Surg., Gynec. & Obst., 130: 1082, 1970. 9. Morse, F. P., III and Dretler, S. P.: Diagnosis and treatment of colovesical fistula. J. Urol., 111: 22, 1974. 10. Prokop, E. K., Buddemeyer, E. U., Strauss, H. W. and Wagner, H. N., Jr.: Detection and localization of an occult vesicoenteric fistula. Amer. J. Roentgen., 121: 811, 1974.