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Intraabdominal abscess in Crohn's (ileo) colitis
Intraabdominal Abscess in Crohn’s (Ileo) Colitis
Adtlan J. OmensteIn, MD, New York, New York DavM B. Sachar, MD, New York, New York Robert J. Qreensteln, MD, New York, New York Hem‘y D. Janowitz, MD, New York, New York Arthur H. A&es,
Jr., MD, New York, New York
Because of the transmural nature of Crohn’s disease, fistulization occurs relatively often. We have noted this ~mp~cation in up to 39 percent of patients [I]. This tendency to fistula formation often results in subacute microperforation with abscess formation. From a series of 230 patients with Crohn’s disease, we studied the clinical features of 46 patients (20 percent) who underwent operations for intraabdominal abscess. Material and Methods The case records of 46 operated patients in whom spontaneous or postoperative intraabdominal abscess occurred during the course of Crohn’s disease were reviewed. These 46 cases were identified among the records of 230 patients, 174 patients with ileocolitis and 56 with Crohn’s colitis, obtained from the computer register of the Mount Sinai Hospital for the period 1964 to 1974. The diagnostic criteria in the selection of these 230 case8 were discussed in detail in earlier reporta [2,3] and are baaed on features describedby Lo&art-Mummery [4], Lindner [5], Korelitz [S], Cook [7], and their co-workers. The diagnosis of intr~~ominal abscess was established by the finding of frank purulent fluid at laparotomy in all 46 patients.
Results Operation for intraabdominal abscess was carried out in 46 (20 percent) of the 236 patients, 9 of 56 with ~~~0~~~ colitis (16 percent) and 37 of 1’74with granulomatous ileocolitis (23 percent). There were more female than male patients in the abscess group (28 versus 18), but this sex distribution was not significantly different from that in the total series (120 to 110). The mean age at the onset of Crohn’s disease was approximately the same in the group of patients Fromlfmf3qWnmtofsvgsrY,hfountsb\aiSctioolofMedici~oftheCIty Unhwsity of New York, and the Mount Slnai Hospital, New York. New York. Requem fw refwints shoukl be akbmed to Adrian J. Greenstein, M), cwpmmt of Surgery, fblwnt Sinai MxlM Center, One Gustave L. Levy Place, 100th Street and Fifth Avenue, New York, New York 10029.
Volume f42. June 1982
with abscess (28 years) as in the nonabscess group (25 years). The mean interval from onset of disease to development of abscess was 10 years (range 1 to 43). There were no important differences in the anatomic distribution of Crohn’s disease in the patients with abscess and those without. The sites of origin of 49 abscesses occurring in the 46 patients are shown in Figure 1(3 patients had 2 separate metachronous abscesses at different sites). Twenty-nine of the abscesses (59 percent) originated in diseased small bowel, while 16 (33 percent) were of colonic origin. The remaining four developed postoperatively adjacent to an ileocolonic suture line. Abscesses were associated with internal or external fistulas in 34 of the 46 patients (75 percent). The sites of presentation and hence of drainage of the 49 abscesses are shown in Figure 2. In five of the nine colitis patients, the origin was the sigmoid colon and the presentation left-sided. In patients with ileocolitis, abscesses were most frequently of ileal origin and presented in the right lower quadrant; they originated from the colon in only three instances. In addition, there were six pelvic abscesses, usually associated with ileo- or colovesical fistulas, and three periumbilical abscesses, two originating in the transverse colon. The epigastric mass, which drained midway between the sternum and the umbilicus, was an anatomic curiosity, since it tracked to this region from ileocecal disease; the transverse colon was normal both on roentgenography and on subsequent laparotomy. The left subphrenic abscess originated in a leaking suture line. Several clinical features more commonly characterized the 46 patients with abscess than the other 134 patients in the series: abdominal mass (55 versus 19 percent,
p
obstruction
(45
versus 29 percent, p <0.025), and fistulas, both internal (49 versus 29 percent, p <0.005) and external (26 versus 9 percent, p
727
Greenstein et al
abscea#wh4opatientswtthCrohn’s F@rei.!Sltoofot&lnd~ (ho) fxntk. The asterkdr Indkates anastomotk oflgln.
Ftgwe 2. Cllnkai stte of pesentatton of 49 abscesses In 46 pattents wtth CmtWs (ho) colttts.
was significantly less common in the abscess group (17 versus 39 percent, p
ately (less than 1 month) after resection or bypass in association with residual or recurrent disease. The two postoperative abscesses in colitis patients developed immediately after ileostomy with exclusion in one case, and within 1 year of partial colectomy with colocolostomy in the other. Abscesses seemed to develop later after bypass (mean 9.6 years) than after resection (mean 2.1 years), but this observation may in part reflect a longer period of follow-up in patients with bypass, a procedure carried out more frequently in earlier years at this hospital [8]. The 46 patients in this series underwent a variety of surgical procedures for their abscesses, with a corresponding variety of results (Figure 3). Simple incision and drainage was carried out as a primary procedure in 24 patients without mortality, but this treatment proved definitive in only 5; the other 19 patients had continuing complications. Eleven pa-
230 PATIENTS 174
46
2’4 SIMPLE INCISION AND DRAINAGE 5 Satisfactory I I Resection! satisfactory 5 Enterocutancous fistuloe 3 Recurrent abscess I I l D -+ Resection
I I+D' Bypass I Resection t drainage
720
56
ileocolitis I om?,,d
Crohn’s I
colitis
FOR ABSCESS
111
PRIMARY “EN-BLOC”
RESECTtON* IO Sotisfoctory I Death
* + drainage
i ILEOSTOMY DIVERSION I Sotisfoctory 4Resection’ 2 Deaths +
A BYPASS
*
I Satisfactory I Resection) 2 Oeat hs
subsequent resection
Flgvrr,2.ResldbofWpkai-ntof tntraabhmtnal abscess tn 230 pMents. I + 0 = lnctstonand drainage.
The American Journal ol Surgery
Abscess in Crohn’s Colitis
tienta underwent bypass or ileostomy diversion, with drainage of the intraabdominal abscess; 4 died, and 5 required subsequent resection. This high mortality rate probably reflects the choice of such nonresectional procedures for more seriously ill patients. The most satisfactory results were obtained in the 11 patients who had primary en bloc resection of bowel and adjacent inflammatory tissue, with complementary drainage. There was only one death in this group, and no abscess recurrence or enterocutaneous fistula formation during a follow-up period of 1 to 4 years. In this series, 5 of the 46 patients (11 percent) died within 32 days of the surgical procedure. Of these five deaths, one was associated with jejunocolic fistula and spontaneous left-sided paracolonic abscess, one with agranulocytosis, one with ileocutaneous and ileovesical fistulas, one with myocardial infarction, and one with sepsis from the abscess alone. In these five patients, two abscesses occurred spontaneously, one ileal and one colonic, and three occurred after previous bypass surgery. In all five cases the abscesses developed before surgery and persisted afterward, with intraabdominal sepsis and bacteremia culminating in death.
recurrent inflammatory bowel disease after abdominal surgery. The only late abscesses we have encountered, unrelated to recurrent or residual disease, occurred after generalized peritonitis or gross surgical contamination of the peritoneal cavity, but no such instance arose in the 230 patients reviewed in this series. Nagler and Policha [18] reported 11 intraabdominal abscesses in eight patients, and described an interesting anatomic classification. Abscesses defined as “enteroparietal” would clearly be those most suited to the simplest procedure, incision and drainage, whereas the deep “intraloop” abscesses would require concomitant drainage and bypass with or without resection and a loop ileostomy. In recent years we have used ultrasonography and computed tomographic scanning with increasing frequency to localize and occasionally drain percutaneously deep intraabdominal abscesses. With this method we have pccasionally seen a fluid-filled collection, behaving clinically as an abscess, respond to antibiotic therapy and disappear. Early recognition, immediate antibiotic treatment, and early surgery for the progressive case are guidelines for present-day therapy of intraabdominal abscess.
Comments
Summary
In our series, intraabdominal abscess developed in 46 of 230 patients (20 percent). This proportion is within the range found in other large series of patients with regional ileitis [9-151. In a separate unpublished study of 213 patients with ileal Crohn’s disease, we noted intraabdominal abscesses in 39 cases (18 percent). Thus, the predominantly colonic distribution of disease in our patients did not profoundly alter the tendency to abscess formation. We agree with Steinberg et al [15] and Alexander-Williams [16], who suggest that intraabdominal abscess is closely linked with fistula formation and is a result of the “extramural extension of a fissure ulcer.” A fistulous tract, either external or internal, could be demonstrated in 34 of our 46 patients (75 percent). The high incidence of abscess of colonic origin is consistent with our previous findings that 23 percent of all fistulas (excluding rectovaginal fistulas) and 38 percent of external fistulas originated in diseased colon [I]. The 50 percent of abscesses with spontaneous as opposed to postoperative onset in this series was greater than the 22 percent proportion of spontaneous fistulas found by Steinberg et al [15]. This difference might reflect different standards for surgical intervention in the two institutions. However, it may also be related to the fact that in our series all patients had colonic involvement, whereas in the series of Steinberg et al [15] only 25 percent had large bowel disease. Steinberg [15], Burney [ 2 71, and their co-workers described the occurrence of late abscesses unrelated
Operations for intraabdominal abscess were performed in 46 (20 percent) of 230 patients with Crohn’s colitis and ileocolitis treated at the Mount Sinai Hospital during the decade 1964 to 1974. Internal and external fistulas, intestinal obstruction, and abdominal mass occurred significantly more often in patients with intraabdominal abscess, while only overt bleeding was significantly less common. Abscesses were equally divided between 23 patients who had undergone previous surgery and 23 cases of spontaneous onset. In ileocolitis, the most frequent site of origin was the terminal ileum with right lower quadrant abscess, as opposed to a sigmoid origin in colitis with presentation in the left lower quadrant. There was no mortality among 24 patients treated with simple drainage, usually for superficial abscess, but enterocutaneous fistulas persisted in 5 of these patients (21 percent). Four of 11 patients (35 percent) died after undergoing bypass or ileostomy diversion. Among the 31 patients surviving either of these procedures, 18 (60 percent) required subsequent resection of the diseased bowel. By contrast, among 11 patients treated with primary en bloc resection plus drainage, there was only 1 death (9 percent) and no abscess recurrence or chronic enterocutaneous fistula formation during a follow-up period of 1 to 4 years. The high mortality rate after bypass may be explained by the more serious nature of the disease and the preexisting deep intraabdominal abscess and postoperative sepsis. Simple extraperitoneal drainage is a safe procedure associated with an extremely low
Volume 143, June 1982
to
729
Greensteinet al
mortality; however, when feasible, resection of the diseased bowel seems to be the treatment of choice for abscess in patients with Crohn’s colitis and ileocolitis. Acknowledgment: We thank Jean DiCarlo for secretarial assistance, Reuben Devaprasad for obtaining medical records and helping transfer data meticulously to McBee cards, and the members of the Mount Sinai staff who gave follow-up information on their private patients.
7.
8.
9. 10.
References 11. 1. Greenstein AJ. Kark AE, Dreiling DA. Crohn’s disease of the colon. I. Fistula in Crohn’s disease of the colon-classification, presenting features, and management in 83 patiits. Am J Gastroenterol 1974;62:419-29. 2. Greenstein AJ, Dreiling DA, Aufses AH Jr. Crohn’s colitis. IV. Clinical features of Crohn’s (ileo) colitis. Am J Gastroenterol 1975;64:191-9. 3. Greenstein AJ, Janowitz l-0, Sachar DB. The extraintestinal complications of Crohn’s disease and ulcerative colitis: a study of 700 patients. Medicine 1976;55:401-12. 4. Lockhart-Mummery HE, Morson BC. Crohn’s disease (regional enteritis) of the large intestine and its distinction from ulcerative colitis. Gut 1960;1:87-105. 5. Lindnsr AE, Marshak RH, Wolf BS, Janowitz HD. Granulornatous colitis. A clinical study. N Engl J Med 1963;269:379-85. 6. Korelitz BI, Present DH, Alpert LI, Marshak RH, Janowitz HD.
730
12. 13. 14. 15. 16. 17.
18.
Recurrent regional ileitis after ileostomy and colectomy for granulomatous colitis. N Engl J Med 1972;287: 110-4. Cook MG, Dixon MF. An analysis of the reliability detection and diignostlc value of various pathological features in Crohn’s disease and ulcerative colitis. Gut 1973;14:255-62. Greenstein AJ. Sachar DB, Pasternack BS, Janowitz HD. Reoperation and recurrence in Crohn’s colitis and ileocolltis: crude and cumulative rates. N Engl J Med 1975;293:68590. Banks BM, Zetzel L, Richter HS. Mwbidlty and mortality in regional enteritis. Am J Dig Dis 1969;14:369-79. Barber KW, Waugh JM, Beahrs OH, Sauer WG. Indications for and the results of the surgical treatment of regioilal enteritis. Ann Surg 1962; 156:472-82. Colcock BP, Vansant JH. Surgical treatment of regional enteritis. N Engl J Med 1960;262:435-44. C&n BB, Yamis H. Regional enteritis. 2nd ed. New York: Grune 8 Stratton, 1956. Edwards H. Crohn’s disease: an inquiry into its nature and consequences. Ann R Coll Surg Engl 1969;44:121-39. Kyle J. Crohn’s disease. New York: Appleton-Century-Crofts, 1972. Steinberg DM, Cooke WT, Alexander-Williams J. Abscess and fistulae in Crohn’s disease. Gut 1973;14:865-9. Alexander-Williams J. The place of surgery in Crohn’s disease. Gut 1971;12:739-50. Burney RE, Gudjonsson B, Cahow CE, Spiro HM. Late appearance of intraabdominal abscesses after total colectomy for inflammatory bowel disease. Arch Surg 1979;114:195-7. Nagler SM, Policha SM. lntraabdominal abscess in regional enteritis. Am J Surg 1979; 137:350-4.
The Amsrlcan Journal ol Surgery
Adtlan J. OmensteIn, MD, New York, New York DavM B. Sachar, MD, New York, New York Robert J. Qreensteln, MD, New York, New York Hem‘y D. Janowitz, MD, New York, New York Arthur H. A&es,
Jr., MD, New York, New York
Because of the transmural nature of Crohn’s disease, fistulization occurs relatively often. We have noted this ~mp~cation in up to 39 percent of patients [I]. This tendency to fistula formation often results in subacute microperforation with abscess formation. From a series of 230 patients with Crohn’s disease, we studied the clinical features of 46 patients (20 percent) who underwent operations for intraabdominal abscess. Material and Methods The case records of 46 operated patients in whom spontaneous or postoperative intraabdominal abscess occurred during the course of Crohn’s disease were reviewed. These 46 cases were identified among the records of 230 patients, 174 patients with ileocolitis and 56 with Crohn’s colitis, obtained from the computer register of the Mount Sinai Hospital for the period 1964 to 1974. The diagnostic criteria in the selection of these 230 case8 were discussed in detail in earlier reporta [2,3] and are baaed on features describedby Lo&art-Mummery [4], Lindner [5], Korelitz [S], Cook [7], and their co-workers. The diagnosis of intr~~ominal abscess was established by the finding of frank purulent fluid at laparotomy in all 46 patients.
Results Operation for intraabdominal abscess was carried out in 46 (20 percent) of the 236 patients, 9 of 56 with ~~~0~~~ colitis (16 percent) and 37 of 1’74with granulomatous ileocolitis (23 percent). There were more female than male patients in the abscess group (28 versus 18), but this sex distribution was not significantly different from that in the total series (120 to 110). The mean age at the onset of Crohn’s disease was approximately the same in the group of patients Fromlfmf3qWnmtofsvgsrY,hfountsb\aiSctioolofMedici~oftheCIty Unhwsity of New York, and the Mount Slnai Hospital, New York. New York. Requem fw refwints shoukl be akbmed to Adrian J. Greenstein, M), cwpmmt of Surgery, fblwnt Sinai MxlM Center, One Gustave L. Levy Place, 100th Street and Fifth Avenue, New York, New York 10029.
Volume f42. June 1982
with abscess (28 years) as in the nonabscess group (25 years). The mean interval from onset of disease to development of abscess was 10 years (range 1 to 43). There were no important differences in the anatomic distribution of Crohn’s disease in the patients with abscess and those without. The sites of origin of 49 abscesses occurring in the 46 patients are shown in Figure 1(3 patients had 2 separate metachronous abscesses at different sites). Twenty-nine of the abscesses (59 percent) originated in diseased small bowel, while 16 (33 percent) were of colonic origin. The remaining four developed postoperatively adjacent to an ileocolonic suture line. Abscesses were associated with internal or external fistulas in 34 of the 46 patients (75 percent). The sites of presentation and hence of drainage of the 49 abscesses are shown in Figure 2. In five of the nine colitis patients, the origin was the sigmoid colon and the presentation left-sided. In patients with ileocolitis, abscesses were most frequently of ileal origin and presented in the right lower quadrant; they originated from the colon in only three instances. In addition, there were six pelvic abscesses, usually associated with ileo- or colovesical fistulas, and three periumbilical abscesses, two originating in the transverse colon. The epigastric mass, which drained midway between the sternum and the umbilicus, was an anatomic curiosity, since it tracked to this region from ileocecal disease; the transverse colon was normal both on roentgenography and on subsequent laparotomy. The left subphrenic abscess originated in a leaking suture line. Several clinical features more commonly characterized the 46 patients with abscess than the other 134 patients in the series: abdominal mass (55 versus 19 percent,
p
obstruction
(45
versus 29 percent, p <0.025), and fistulas, both internal (49 versus 29 percent, p <0.005) and external (26 versus 9 percent, p
727
Greenstein et al
abscea#wh4opatientswtthCrohn’s F@rei.!Sltoofot&lnd~ (ho) fxntk. The asterkdr Indkates anastomotk oflgln.
Ftgwe 2. Cllnkai stte of pesentatton of 49 abscesses In 46 pattents wtth CmtWs (ho) colttts.
was significantly less common in the abscess group (17 versus 39 percent, p
ately (less than 1 month) after resection or bypass in association with residual or recurrent disease. The two postoperative abscesses in colitis patients developed immediately after ileostomy with exclusion in one case, and within 1 year of partial colectomy with colocolostomy in the other. Abscesses seemed to develop later after bypass (mean 9.6 years) than after resection (mean 2.1 years), but this observation may in part reflect a longer period of follow-up in patients with bypass, a procedure carried out more frequently in earlier years at this hospital [8]. The 46 patients in this series underwent a variety of surgical procedures for their abscesses, with a corresponding variety of results (Figure 3). Simple incision and drainage was carried out as a primary procedure in 24 patients without mortality, but this treatment proved definitive in only 5; the other 19 patients had continuing complications. Eleven pa-
230 PATIENTS 174
46
2’4 SIMPLE INCISION AND DRAINAGE 5 Satisfactory I I Resection! satisfactory 5 Enterocutancous fistuloe 3 Recurrent abscess I I l D -+ Resection
I I+D' Bypass I Resection t drainage
720
56
ileocolitis I om?,,d
Crohn’s I
colitis
FOR ABSCESS
111
PRIMARY “EN-BLOC”
RESECTtON* IO Sotisfoctory I Death
* + drainage
i ILEOSTOMY DIVERSION I Sotisfoctory 4Resection’ 2 Deaths +
A BYPASS
*
I Satisfactory I Resection) 2 Oeat hs
subsequent resection
Flgvrr,2.ResldbofWpkai-ntof tntraabhmtnal abscess tn 230 pMents. I + 0 = lnctstonand drainage.
The American Journal ol Surgery
Abscess in Crohn’s Colitis
tienta underwent bypass or ileostomy diversion, with drainage of the intraabdominal abscess; 4 died, and 5 required subsequent resection. This high mortality rate probably reflects the choice of such nonresectional procedures for more seriously ill patients. The most satisfactory results were obtained in the 11 patients who had primary en bloc resection of bowel and adjacent inflammatory tissue, with complementary drainage. There was only one death in this group, and no abscess recurrence or enterocutaneous fistula formation during a follow-up period of 1 to 4 years. In this series, 5 of the 46 patients (11 percent) died within 32 days of the surgical procedure. Of these five deaths, one was associated with jejunocolic fistula and spontaneous left-sided paracolonic abscess, one with agranulocytosis, one with ileocutaneous and ileovesical fistulas, one with myocardial infarction, and one with sepsis from the abscess alone. In these five patients, two abscesses occurred spontaneously, one ileal and one colonic, and three occurred after previous bypass surgery. In all five cases the abscesses developed before surgery and persisted afterward, with intraabdominal sepsis and bacteremia culminating in death.
recurrent inflammatory bowel disease after abdominal surgery. The only late abscesses we have encountered, unrelated to recurrent or residual disease, occurred after generalized peritonitis or gross surgical contamination of the peritoneal cavity, but no such instance arose in the 230 patients reviewed in this series. Nagler and Policha [18] reported 11 intraabdominal abscesses in eight patients, and described an interesting anatomic classification. Abscesses defined as “enteroparietal” would clearly be those most suited to the simplest procedure, incision and drainage, whereas the deep “intraloop” abscesses would require concomitant drainage and bypass with or without resection and a loop ileostomy. In recent years we have used ultrasonography and computed tomographic scanning with increasing frequency to localize and occasionally drain percutaneously deep intraabdominal abscesses. With this method we have pccasionally seen a fluid-filled collection, behaving clinically as an abscess, respond to antibiotic therapy and disappear. Early recognition, immediate antibiotic treatment, and early surgery for the progressive case are guidelines for present-day therapy of intraabdominal abscess.
Comments
Summary
In our series, intraabdominal abscess developed in 46 of 230 patients (20 percent). This proportion is within the range found in other large series of patients with regional ileitis [9-151. In a separate unpublished study of 213 patients with ileal Crohn’s disease, we noted intraabdominal abscesses in 39 cases (18 percent). Thus, the predominantly colonic distribution of disease in our patients did not profoundly alter the tendency to abscess formation. We agree with Steinberg et al [15] and Alexander-Williams [16], who suggest that intraabdominal abscess is closely linked with fistula formation and is a result of the “extramural extension of a fissure ulcer.” A fistulous tract, either external or internal, could be demonstrated in 34 of our 46 patients (75 percent). The high incidence of abscess of colonic origin is consistent with our previous findings that 23 percent of all fistulas (excluding rectovaginal fistulas) and 38 percent of external fistulas originated in diseased colon [I]. The 50 percent of abscesses with spontaneous as opposed to postoperative onset in this series was greater than the 22 percent proportion of spontaneous fistulas found by Steinberg et al [15]. This difference might reflect different standards for surgical intervention in the two institutions. However, it may also be related to the fact that in our series all patients had colonic involvement, whereas in the series of Steinberg et al [15] only 25 percent had large bowel disease. Steinberg [15], Burney [ 2 71, and their co-workers described the occurrence of late abscesses unrelated
Operations for intraabdominal abscess were performed in 46 (20 percent) of 230 patients with Crohn’s colitis and ileocolitis treated at the Mount Sinai Hospital during the decade 1964 to 1974. Internal and external fistulas, intestinal obstruction, and abdominal mass occurred significantly more often in patients with intraabdominal abscess, while only overt bleeding was significantly less common. Abscesses were equally divided between 23 patients who had undergone previous surgery and 23 cases of spontaneous onset. In ileocolitis, the most frequent site of origin was the terminal ileum with right lower quadrant abscess, as opposed to a sigmoid origin in colitis with presentation in the left lower quadrant. There was no mortality among 24 patients treated with simple drainage, usually for superficial abscess, but enterocutaneous fistulas persisted in 5 of these patients (21 percent). Four of 11 patients (35 percent) died after undergoing bypass or ileostomy diversion. Among the 31 patients surviving either of these procedures, 18 (60 percent) required subsequent resection of the diseased bowel. By contrast, among 11 patients treated with primary en bloc resection plus drainage, there was only 1 death (9 percent) and no abscess recurrence or chronic enterocutaneous fistula formation during a follow-up period of 1 to 4 years. The high mortality rate after bypass may be explained by the more serious nature of the disease and the preexisting deep intraabdominal abscess and postoperative sepsis. Simple extraperitoneal drainage is a safe procedure associated with an extremely low
Volume 143, June 1982
to
729
Greensteinet al
mortality; however, when feasible, resection of the diseased bowel seems to be the treatment of choice for abscess in patients with Crohn’s colitis and ileocolitis. Acknowledgment: We thank Jean DiCarlo for secretarial assistance, Reuben Devaprasad for obtaining medical records and helping transfer data meticulously to McBee cards, and the members of the Mount Sinai staff who gave follow-up information on their private patients.
7.
8.
9. 10.
References 11. 1. Greenstein AJ. Kark AE, Dreiling DA. Crohn’s disease of the colon. I. Fistula in Crohn’s disease of the colon-classification, presenting features, and management in 83 patiits. Am J Gastroenterol 1974;62:419-29. 2. Greenstein AJ, Dreiling DA, Aufses AH Jr. Crohn’s colitis. IV. Clinical features of Crohn’s (ileo) colitis. Am J Gastroenterol 1975;64:191-9. 3. Greenstein AJ, Janowitz l-0, Sachar DB. The extraintestinal complications of Crohn’s disease and ulcerative colitis: a study of 700 patients. Medicine 1976;55:401-12. 4. Lockhart-Mummery HE, Morson BC. Crohn’s disease (regional enteritis) of the large intestine and its distinction from ulcerative colitis. Gut 1960;1:87-105. 5. Lindnsr AE, Marshak RH, Wolf BS, Janowitz HD. Granulornatous colitis. A clinical study. N Engl J Med 1963;269:379-85. 6. Korelitz BI, Present DH, Alpert LI, Marshak RH, Janowitz HD.
730
12. 13. 14. 15. 16. 17.
18.
Recurrent regional ileitis after ileostomy and colectomy for granulomatous colitis. N Engl J Med 1972;287: 110-4. Cook MG, Dixon MF. An analysis of the reliability detection and diignostlc value of various pathological features in Crohn’s disease and ulcerative colitis. Gut 1973;14:255-62. Greenstein AJ. Sachar DB, Pasternack BS, Janowitz HD. Reoperation and recurrence in Crohn’s colitis and ileocolltis: crude and cumulative rates. N Engl J Med 1975;293:68590. Banks BM, Zetzel L, Richter HS. Mwbidlty and mortality in regional enteritis. Am J Dig Dis 1969;14:369-79. Barber KW, Waugh JM, Beahrs OH, Sauer WG. Indications for and the results of the surgical treatment of regioilal enteritis. Ann Surg 1962; 156:472-82. Colcock BP, Vansant JH. Surgical treatment of regional enteritis. N Engl J Med 1960;262:435-44. C&n BB, Yamis H. Regional enteritis. 2nd ed. New York: Grune 8 Stratton, 1956. Edwards H. Crohn’s disease: an inquiry into its nature and consequences. Ann R Coll Surg Engl 1969;44:121-39. Kyle J. Crohn’s disease. New York: Appleton-Century-Crofts, 1972. Steinberg DM, Cooke WT, Alexander-Williams J. Abscess and fistulae in Crohn’s disease. Gut 1973;14:865-9. Alexander-Williams J. The place of surgery in Crohn’s disease. Gut 1971;12:739-50. Burney RE, Gudjonsson B, Cahow CE, Spiro HM. Late appearance of intraabdominal abscesses after total colectomy for inflammatory bowel disease. Arch Surg 1979;114:195-7. Nagler SM, Policha SM. lntraabdominal abscess in regional enteritis. Am J Surg 1979; 137:350-4.
The Amsrlcan Journal ol Surgery