Gut, 1974, 15, 845-851

Excisional surgery with ileostomy for Crohn'scolitis with particular reference to factorsaffecting recurrence

D. M. STEINBERG1, R. N. ALLAN, H. THOMPSON, B. N. BROOKE2,J. ALEXANDER-WILLIAMS3, AND W. T. COOKE

From the Nutritional and Intestinal Unit, The General Hospital, Birmingham

SUMMARY This paper reports the indications for, and results of, excision of the large intestine withileostomy in 73 patients with Crohn's colitis who have been followed for a mean of nine years sinceresection. Sixty-four of them are still alive and all but two of the survivors are now in good health.

However, 23 (33 %) have developed recurrent Crohn's disease since resection. This is higher thanthat reported in many other series and may be due to differences in the length of follow up, the siteand extent of colonic disease, the age of the patient at the time of excision with ileostomy, anddifferences in the pathological interpretation of the diagnosis of Crohn's disease. The high recurrencerate in this series lends caution to the view that the prognosis after excisional surgery and ileostomyfor Crohn's colitis is as good as after the same operation for ulcerative colitis and should influencethe decision when the alternative of medical or surgical management are being considered forpatients with Crohn's colitis.

The medical management of Crohn's colitis fre-quently fails to control symptoms (Howel-Jones,Lennard-Jones, and Lockhart-Mummery, 1966)and operative treatment either by defunctioningileostomy or ileo-rectal anastomosis has not beenentirely satisfactory (Burman, Cooke, and Williams,1971). Proctocolectomy with ileostomy has beenclaimed to be effective in restoring patients withsevere disease to good health (Ritchie and Lockhart-Mummery, 1973) but there is some doubt as to theincidence of recurrence of Crohn's disease after thisoperation. A 7% incidence is reported by Ritchieand Lockhart-Mummery (1973) from St Mark'sHospital and 11 % by De Dombal, Burton, andGoligher (1971) from Leeds. Nugent, Veidenheimer,Meissner, and Haggitt (1973) from the Lahey Clinicfound only one recurrence (3.6 %) after generalsurgery and ileostomy in 28 patients followed for10 to 15 years. Such reports seem to confirm earlyconcepts that Crohn's disease could remain confinedto the large bowel and that therefore low recurrence

'Supported by a Raine travelling scholarship of the University ofWestern Australia

'St George's Hospital, London

9External scientific staff, Medical Research Council

Received for publication 27 June 1974.

rates should follow excision of the colon (Wells,1952; Brooke, 1959; Lockhart-Mummery andMorson, 1960). In contrast, Korelitz, Present, Alpert,Marshak, and Janowitz (1972) have shown a 46%recurrence rate when Crohn's colitis was treated byexcision with ileostomy.

This paper reports the indication for, and resultsof, surgery in 73 patients having excisional surgerywith ileostomy for Crohn's colitis between 1950 and1972 and the incidence of recurrent disease, andincludes a discussion of the factors which mightexplain the striking differences between the recur-rence rates in this and other reported series.

Materials and Methods

The clinical, radiological, and pathological criteriafor distinguishing ulcerative colitis and Crohn'scolitis are identical to those of Lockhart-Mummeryand Morson(1960and 1964)andofLindner, Marshak,Wolf, and Janowitz (1963). The criteria for thediagnosis of recurrence have been based on histologyafter surgical resection in all but three patients whohave characteristic radiological changes.The results of excisional surgery with ileostomy

for Crohn's colitis have been analysed in a consecu-tive series of 418 patients with Crohn's diseasetreated at the General Hospital, Birmingham,

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846 D. M. Steinberg, R. N. Allan, H. Thompson, B. N. Brooke, J. Alexander- Williams, and W. T. Cooke

between 1942 and 1973. The disease affected thesmall bowel alone in 2q4, the large and small bowelin 136, and the large bowel alone in 68. Of the 204patients with large bowel involvement, 73 (40 menand 33 women) were treated by excisional surgerywith ileostomy.The mean age at onset of symptoms in men was

27.2 years (range 13-67 years) and 21.6 years(range 11-40 years) in women. Forty-two patientsran a course of continuous symptoms with diarrhoea,abdominal pain, general malaise, and weight losswhile 29 ran a chronic intermittent course. Two ofthem presented with acute fulminating disease. Therewas a mean interval of 6.1 years between the onset ofsymptoms and excisional surgery with ileostomy.Twenty-seven patients had had a previous bowelresection (table I).

None . . 46Distal ileum.2Right hemicolectomy ... 9Left hemicolectomy ..3Multiple segmental resection . .. 3Ileo-rectal anastomosis .. . .10

Table I Previous surgery in patients undergoingexcisional surgery with ileostomy

Operation was usually undertaken when medicaltreatment or previous surgery had failed to controlsymptoms. Thirty-eight patients were submitted tosurgery because their symptoms persisted despitecorticosteroid therapy. Contributory factors includedthe presence of perianal disease in 30 patients (inseven florid perianal disease was the main indicationfor excision), six had obstructive features, twofistulae, and one acute dilatation of the colon.The extent of colonic involvement is shown in

table II. In 38 of the 73 patient the distal small bowelwas involved. Thirty-six patients were treated by a

one-stage panproctocolectomy, while five had a two-stage procedure. Early in the series 12 patients weretreated by a temporary ileostomy followed later bya panproctocolectomy. Seven patients had colec-tomy with ileostomy where the proximal rectumwas exteriorized as a mucous fistula and three had acolectomy, ileo-rectal anastomosis, and a defunc-tioning ileostomy. Ten patients treated previouslyby ileo-rectal anastomosis were submitted to excision

Total colon and rectum .. . . 54Total colon with rectal sparing 7

Left side only. 9Right side only . 1Not known. 2

Table TI Extent of colonic involvement

of the rectum with ileostomy because of persistentdiarrhoea, general malaise, and perianal sepsis.

Results

MORBIDITY AND MORTALITY

Operative mortalityThree of the 73 patients died, an operative mortalityrate of 4.1 %. Two developed peritonitis complicatedby septicaemia and bronchopneumonia and one

died from a massive haemorrhage due to a disorderof coagulation.

Early morbidityTwenty-four experienced ileostomy dysfunction(either mechanical obstruction or profuse ileostomyoutput) in the first four weeks after excisional surgeryand six were treated surgically for the relief of mech-anical obstruction either at or immediately proximalto the stoma. The commonest site of sepsis was theperianal wound after proctectomy which occurredin 21 out of 64 patients. Six had major peritonealsepsis and eight major abdominal wound infections.

Late mortalityThe late mortality related to the disease was 7.1%(5 out of 70), four of whom died after resection ofrecurrent disease (see below) and the other afterinsertion of a T tube for stenosing cholangitis. Therewas one additional but unrelated death due to cere-brovascular disease.

Late morbidityAll the survivors have been reviewed regularly withrecent clinical, radiological, biochemical, andhaematological assessment. The mean duration offollow up since ileostomy was 8.7 years. During thistime 45 (64 %) of the 70 patients followed have beenre-admitted on 96 occasions (table Ill).

RECURRENT DISEASE

Recurrence rateTwenty-three have had evidence of recurrent disease,

Recurrence (treated surgically) .29Ileostomy reconstruction (no recurrence) .20Ileostomy flux .23Obstruction due to adhesions. 9Perianal sepsis. 3Weakness and anaemia. 2Jaundice . . 1Other operations. 9Total 96

Table III Causes of readmission after excisionalsurgery with ileostomy in 45 patients with Crohn'sdisease

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Excisional surgery with ileostomyfor Crohn's colitis withparticular reference tofactors affecting recurrence 847

a recurrence rate of 33%. Twenty (29%) have hadfurther resections for histologically proven recurrentdisease on 25 occasions. Three others, and one patientwho has already had a resection for recurrent diseasehave radiological evidence of recurrence.

Table IV shows the principal clinical features.Subacute obstruction, occurring at or just proximalto the stoma, was the major feature in nearly half thepatients. Obstruction was associated with intermit-tent profuse ileostomy output in eight patients, withovert bleeding in three, and in two was complicatedby a perforation of the terminal ileum. Five of thisgroup presenting with obstructive features hadrecurrence at the stoma with ulcers, stenosis, orcutaneous fistulae. Abscess and fistula was the modeof presentation on seven occasions: four throughparamedian scars, one at a right subcostal drainsite, and two adjacent to the ileostomy. Three ofthese episodes were due to jejunal recurrence in twopatients.

Obstructive pattern 13Bleeding (anaemia) 2Abscess/fistula. 7Stomal problems only. 2Flux problems only 3Weight loss, general poor health 1Dyspepsia . . 1Total recurrences .29

Table IV Presentation of recurrent proximal disease

X-ray diagnosisIn 23 of the 29 episodes of recurrence a bariumfollow-through combined with a limited ileostomyenema showed radiological abnormality, usually anarrow segment of the terminal ileum with proximaldilatation. Demonstrations of external fistulae weresuccessful using a combined sinogram follow-through technique to demonstrate the connexion andalso the extent of any underlying disease. Recurrentdisease was found at laparotomy on six occasionsdespite negative radiology, emphasizing the difficultyof radiological demonstration of the ileum im-mediately proximal to the stoma.

Laboratory investigationsHaematological and/or biochemical abnormalitiesat the time of recurrence were present in 17 patients:three were only anaemic (haemoglobin <12 g%)while 14 (60%) had biochemical evidence of activedisease (albumin <4 g% and seromucoids >150mg %).

Site of recurrenceThe site of recurrence is shown in table V. Disease

Terminal ileum .20Diffuse small bowel. 5Jej anal. 3Gastric (antral). 1

Table V Site of recurrent disease (29 recurrences)

involving the terminal ileum is defined as that occur-ring within 25 cm of the stoma. Of the five withextensive small bowel disease one had jejunal andileal disease and the others diffuse involvementconfined to the ileum. One patient had a gastricrecurrence initially misdiagnosed as a prepyloriculcer.

HistopathologyPathological examination was performed on theresected specimens in 20 patients. In all but two thehistological material has been reviewed by one ofthe authors (H.T.). Epithelioid follicles with Lang-han's giant cells were identified in 14. Of the remain-ing six there were transmural inflammation andfissuring in four and in the other two from whomtissue was no longer available for study the patho-logical reports written at the time favoured adiagnosis of recurrent Crohn's disease.

TREATMENT OF RECURRENCETwenty ofthe 23 patients with recurrence have under-gone 26 resections. Excision of the terminal ileumwith refashioning of the ileostomy was performedon 20 occasions and a proximal resection on fouroccasions (three times in the same person all forjejunal disease. A gastric recurrence was treatedinitially with vagotomy and pyloroplasty butsymptoms persisted until an antrectomy produced asatisfactory result.Four patients (including one who has already had

a resection for recurrent disease) have extensivesmall bowel involvement demonstrated radiologi-cally. Three are receiving ACTH, and the other, withrecurrent bleeding, haematinics only. All four arenow symptomatically controlled and two of themhave shown radiological and biochemical improve-ment.

Mortality from recurrent diseaseFour patients died after operations for recurrentdisease: three following resections of the ileum (twowith fistulae complicating perforation and one withextensive disease) and another after a diagnosticlaparotomy at which irresectable diffuse smallintestinal involvement was found. Deaths were dueto septicaemia, electrolyte imbalance, or pulmonaryemboli.

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848 D. M. Steinberg, R. N. Allan, H. Thompson, B. N. Brooke, J. Alexander-Williams, and W. T. Cooke

FACTORS AFFECTING RECURRENCE RATE

Lenigth offollow upIn our series the majority of recurrences haveoccurred within five years (14 of 23), the remainderoccurring at varying intervals up to 19 years afterileostomy (fig 1). A cumulative recurrence graphdemonstrating the wide scatter in the length offollow up is shown in figure 2. The recurrence riskis considered as the percentage of the number ofrecurrences against the total number of patientsfollowed in each particular year. There was a 10%incidence in the first year and thereafter an annual5%. risk a cumulative incidence to 100% at 18years. All six patients followed for more than 15years after ileostomy have suffered at least onerecurrence.

Site and extent of diseaseFifty-three per cent had histologically confirmed

1 00 3/3

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u 50 7/17

9z 2/9

D,25

<1 YR . 1-5YRS . 5-IOYRS. >1 OYRS

TIME BETWEEN ONSET OF DISEASE & LEOSTOMY

Fig 1 Time interval for recurrence after ileostomy andcolectomy.

ileal involvement at the time of excisional surgery.There was no significant difference in the risk ofdevelopment of recurrence whether or not the ileumwas involved. Thirteen recurrences occurred in 37patients with initial ileal involvement compared with10 recurrences in 33 patients whose ileum was con-sidered normal.The patients have been divided into three groups:

those whose large bowel was wholly involved, thosewith disease confined to the left side, and those withright-sided disease.

If only colonic involvement is considered whetherthe small intestine is involved or not (table VI) thenin those with left-sided disease all six recurred morethan five years after surgery (fig 3), whilst 15 of 17recurrences with total colonic involvement occurredwithin five years of ileostomy.

Total Right- Left-Involvement sided sided

Birmingham series(75 patients) 83% 2% 15%

St Mark s series(90 patients) 53% 3% 44%

Table VI Distribution of colonic Crohn's disease inpatients receiving non-restorative surgery for Crohn'sdisease'Ileostomy and colostomy

PATI E NTS

3

56

0 RECURRENCE

5 10YEARS OF FOLLOW-UP

1 5

ANNUAL RISK - 5%

Fig 3 The development of recurrence in patientstreated by ileostomy and colectomy for Crohn's diseaseconfined to left side of colon.

Age at excisional surgeryThe mean age at the time of excisional surgery withileostomy was 33-3 years. The incidence of recur-rence compared with age at excisional surgery withileostomy is shown in a cumulative recurrence graphfor patients above and below the age of 40 at thetime of excisional surgery and ileostomy (fig 4).The younger group had both an initially higherincidence of recurrence and a higher annual incidencesubsequently.

70

60

50

40

30

20

!0

5 10 15 20 25YEARS AFTER SURGERY

Fig 2 Cumulative recurrence graph after ileostomyand colectomy.

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ABOVE 40 _100 BELOW 40 -

90

80

70

60

50 -

40 £ - -

30 -

20 -0

10 -

S 10 15 20YEARS AFTER SURGERY

Fig 4 A comparison of cumulative recurrence riskabove and below the age of40.

Duration of disease before excisional surgery andileostomyAccording to the interval between the onset ofsymptoms and the time of excisional surgery andileostomy, the patients have been divided into fourgroups. The incidence of recurrence in each groupfive years after surgery is shown in figure 5. Thenumbers in each group are too small for statisticalcomparison but suggest a trend towards a higherrecurrence risk with a shorter length of historybefore excisional surgery.

v

I-a.

U-

0 3

Z 2

5 10 15YEARS AFTER FIRST OPERA

Fig 5 The incidence of recurrence at five yearcompared with varying duration of disease befoileostomy and colectomy.

Era and surgeonUntil 1963 the operations were performed by oneauthor (B.N.B.) and since then by another (J.A.W.).This allows a convenient division of the series intotwo eras. The crude overall recurrence rate appearsto indicate a higher recurrence rate in the first era(table VII). However, a comparison of the recurrencerate in those patients followed for five years afterresection shows that there was no significantdifference between the two and that it is easy to bemisled by considering crude recurrence rates inisolation from the length of follow up.

Recurrence Surgeon Era Surgeon EraB.N.B. 1947-1963 J.A.W. 1963-1973

OverallNumber of patients 32 38Total recurrence to date 14 (44%) 9 (24%)At five yearsNumber of patients 32 20Recurrence at 5 years 7 (22%) 6 (30%)

Table VII Recurrence rates in the two surgical eras

One-stage or multiple operationsThe risk of recurrence was the same if the operationwas done as a one-stage panproctocolectomy or amultiple-staged procedure. Ten of the 35 patientstreated by a one-stage panproctocolectomy developedrecurrence of disease compared with 13 of the 35undergoing multiple staged procedures. There wasan equal distribution of single and multistagedoperations in this centre between 1950 and 1972.Furthermore, there was no significant difference inthe risk of proximal recurrence if the rectum wasleft in situ at the time of colectomy (two recurrencesin nine patients).

CURRENT STATUS OF ALL PATIENTSSixty-four of the original 73 patients are still alive,including 19 of the 23 who have had recurrentdisease.

All but one of these 19 are currently in goodhealth; however, three of them have previouslyexperienced such prolonged illness and hospitaltreatment that their overall course since ileostomycan hardly have been considered satisfactory, whileeight (four with radiological recurrence) suffer minordisability from episodes of profuse ileostomy outputand anaemia but are nevertheless considered to be in

20 good health because their symptoms are well con-kTI0N trolled and they are at work.Is The other 45 are all well except one patient withwre an obsessional neurosis which antedates the onset of

the Crohn's disease.

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850 D. M. Steinberg, R. N. Allan, H. Thompson, B. N. Brooke, J. Alexander-Williams, and W. T. Cooke

Of the 64 survivors, 36 are taking supplements ofpotassium, iron, and folic acid, and eight are stillreceiving steroid therapy. Fifty patients (78 %) werewithin normal limits as regards haematological andbiochemical status (haemoglobin > 12.0 g%; albu-min > 4 g%; seromucoids < 150 mg%); 14 (22%)showed abnormality in one or more respects.

Discussion

One third of our patients with Crohn's disease of thelarge bowel were treated by excisional surgery withileostomy. The operative mortality rate of 4.1 % issimilar to that reported from other centres. DeDombal et al (1971) reported an operative mortalityrate of 51 % (two deaths out of 39) and Ritchie andLockhart-Mummery (1973) 31 % (two deaths outof 64) for patients treated by panproctocolectomywith ileostomy. Although there is a fairly lowoperative mortality rate there is a much higher earlymorbidity rate due to ileostomy dysfunction whencompared with panproctocolectomy for ulcerativecolitis and a higher late morbidity due to recurrenceand further surgery (Steinberg, Allan, Brooke,Cooke, and Alexander-Williams, 1974).

Recurrent disease after excisional surgery withileostomy has only previously been reported in theterminal ileum (Goligher, 1972; Ritchie andLockhart-Mummery, 1973) whereas only 70% of ourrecurrences have occurred at this site. Our experiencein finding evidence of recurrence in the upper intestineis unusual, five developing extensive small boweldisease, three jejunal lesions, and one a gastriclesion.

Careful consideration has been given to thediagnosis of non-specific prestomal ileitis (Turnbull,Weakley, and Farmer, 1964; Knill-Jones, Morson,and Williams, 1970) but none of our patientsappeared to fulfil their criteria. Furthermore, manyof those followed by Turnbull have subsequentlyshown a high incidence of recurrent Crohn's disease(Goligher, 1967). In our view recurrent ileitis afterexcisional surgery is due to recurrent Crohn'sdisease irrespective of whether or not the ileum wasinitially involved.

In contrast to the experience of Nugent andcolleagues (1973) and Glotzer, Gardner, Goldman,Hinnichs, Rosen, and Zetzel (1970), 11 (48 %) of our23 patients with recurrent disease presented a majormanagement problem. Four died after an operationfor recurrent disease; five had diffuse small bowel re-currence with systemic upset, and two with jejunal re-currence were complicated by abscess and fistulae.However, despite multipleoperations insome ofthem,the overall present health of the survivors is not asbad as that described by Korelitz et al (1972) who

reported that only 45% were well and that 191 werecrippled by complications.Our findings are in accordance with those of

Kiefer, Marshall, and Brolsma (1951) and Fielding,Cooke, and Williams (1972) that the incidence ofrecurrence is related to the length of follow up. Thismay explain the difference from the study of DeDombal et al (1971) where the follow up periodafter panproctocolectomy for Crohn's colitis wasshort. Furthermore, Goligher (1972) only one yearlater reported further patients in this series who haddeveloped recurrent Crohn's disease.The different recurrence rates in this and the

reported series of Ritchie and Lockhart-Mummery(1973) are not so simply explained. However, thedistribution of colonic disease was different as alarge number of patients with predominantly left-sided colonic disease were seen at St Mark's Hospitalcompared with our series (table VI). Ritchie andLockhart-Mummery (1973) state that the patientswith distal colonic disease have a better overallprognosis following excision and ileostomy orcolostomy. Our experience of a smaller group withleft-sided colonic disease suggests that in generalthose patients with disease limited to the leftcolon have an equal risk of developing recurrence tothose with diffuse colonic disease.We found a much higher incidence of ileal

involvement at the initial operation (53 %) comparedwith the'r series (30%). However, we did not findany significant difference in the recurrence ratewhether or not the ileum was involved at the time ofexcisional surgery, nor can we support the conten-tion of McGovern and Goulston (1968) that granu-lomatous colitis with involvement of the terminalileum behaves in a more benign manner than if thedisease is confined to the colon. De Dombal et al(1971) suggest that the younger the patient at thetime of the first operation the greater the risk ofrecurrence and our results support this suggestion.This may explain the difference between the 33%recurrence rate in this series and the 7% reported byRitchie and Lockhart-Mummery (1973) with meanages at operation of 31.5 years and 39 years respec-tively. Our findings do not support their view thatrecurrence was more likely to occur after a stagedoperation than after a panproctocolectomy. Theapparent difference between the two series can bestbe explained by considering the length of follow up.Most of the staged procedures reported by Ritchieand Lockhart-Mummery (1973) were performedduring the early years of their experience and havetherefore been followed for a longer period with agreater risk of developing recurrence than thosepatients undergoing a one-stage panproctocolectomy.

Excisional surgery with ileostomy has proved an

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Excisional surgery with ileostomyfor Crohn's colitis withparticular reJerence tofactors affecting recurrence 851

effective method of treating extensive Crohn'sdisease of the large bowel where medical manage-ment has been unsuccessful in controlling symptoms.The operation should not be undertaken lightly, forpatients even with total colonic involvement mayremain well for many years with conservative treat-ment alone (Allan, Steinberg, Williams, and Cooke,1974).Unlike those patients with ulcerative colitis,

excisional surgery with ileostomy for Crohn'sdisease cannot guarantee a cure but most patientsremain in good health apart from a small group whoexperience transient episodes of ileostomy dys-function. Nearly all those patients who havedeveloped recurrent disease and undergone furtherresections have been restored to good health.

References

Allan, R. N., Steinberg, D. M., Williams, J. A., and Cooke, W. T.The medical management of Crohn's colitis. (In preparation).

Brooke, B. N. (1959). Granulomatous diseases of the Intestine. Lancet2, 745.

Burman, J. H., Cooke, W. T., and Williams, J. A. (1971). Fate ofileorectal anastomosis in Crohn's disease. Gut, 12, 432-436.

De Dombal, F. T., Burton, I., and Goligher, J. C. (1971). Recurrenceof Crohn's disease after primary excisional surgery. Gut, 12,519-527.

Fielding, J. F., Cooke, W. T., and Williams, J. A. (1972). The incid-ence of recurrence in Crohn's disease. Surg. Gynec. Obstet.,134, 467-469.

Glotzer, D. J., Gardner, R. C., Goldman, H., Hinrichs, H. R., Rosen,H., and Zetzel, L. (1970). Comparative features and course ofulcerative and granulomatous colitis. New Engl. J. Med., 282,582-587.

Goligher, J. C. (1967). Surgery ofAnus, Rectum and Colon, 2nd ed.,p. 938. Bailliere, Tindall, and Cassell, London.

Goligher, J. C. (1972). Ileal recurrence after ileostomy and excisionof the large bowel for Crohn's disease. Brit. J. Surg., 59,253-269.

Howel-Jones, ,J., Lennard-Jones, J. E., and Lockhart-Mummery,H. E. (1966). Experience in the treatment of Crohn's disease ofthe large intestine. Gut, 7, 448-452.

Kiefer, E. D., Marshall, S. F., and Brolsma, M. P. (1950). The manage-ment of chronic regional ileitis. Gastroenterology, 14, 118-130.

Knill-Jones, R. P., Morson, B., and Williams, R. (1970). Prestomalileitis: clinical and pathological findings in five cases. Quart. J.Med., 39, 154, 287-297.

Korelitz, B. I., Present, D. H., Alpert, L. I., Marshak, R. H., andJanowitz, H. D. (1972). Recurrent regional ileitis after ileos-tomy and colectomy for granulomatous colitis. New Engl. J.Med., 287, 110-1 15.

Lindner, A. E., Marshak, R. H., Wolf, B. S., and Janowitz, H. D.(1963). Granulomatous colitis: a clinical study. New Engl. J.Med., 269, 379-385.

Lockhart-Mummery, H. E., and Morson, B. C. (1960). Crohn'sdisease (regional enteritis) of the large intestine and its dis-tinction from ulcerative colitis. Gut, 1, 87-105.

Lockhart-Mummery, H. E., and Morson, B. C. (1964). Crohn'sdisease of the large intestine. Gut, 5, 493-509.

McGovern, V. J., and Goulston, S. J. M. (1968). Crohn's disease ofthe colon. Gut, 9, 164-176.

Nugent, F. W., Veidenheimer, M. C., Meissner, W. A., and Haggitt,R. C. (1973). Prognosis after colonic resection for Crohn'sdisease of the colon. Gastroenterology, 65, 398-402.

Ritchie, J. K., and Lockhart-Mummery, H. E. (1973). Non-restorativesurgery in the treatment of Crohn's disease of the large bowel.Gut, 14, 263-269.

Steinberg, D. M., Allan, R. N., Brooke, B. N., Cooke, W. T., andAlexander-Williams, J. (1974). The sequelae of colostomy andileostomy: comparison between Crohn's colitis and ulcerativecolitis. Gastroenterology, in press.

Tumbull, R. B., Jr., Weakley, F. L., and Farmer, R. G. (1964).Ileitis after colectomy and ileostomy for non-specific ulcerativecolitis. Dis. Colon Rect., 7, 427-438.

Wells, C. (1952). Ulcerative colitis and Crohn's disease. Ann. roy.Coll. Surg. Engl., 11, 105-120.

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