Late Onset Crohn's Disease in Patients with Colonic Diverticulitis* IRWIN R. BERMAN, M.D.t, MARVIN L. CORMAN, M.D., MALCOLM C. VEIDENHEIMER, M.D.

JOHNA. COLLER, M.D.,

From the Section of Colon and Rectal Surgery, Lahey Clinic Foutzdation, Boston, Massachusetts

PATIENTS "WHOREQUIRE colonic resection for diverticulitis seldom require a second operation for recurrence o f this disease. 1 Recently we p e r f o r m e d a second colonic resection for a patient who had r e c u r r e n t pain, fever, and abdominal tenderness two years after resection o f the sigmoid colon for diverticulitis. Alt h o u g h the clinical and intraoperative impression in this patient was diverticulitis, histopathologic examination o f the second resected specimen showed colonic Crohn's disease as well as diverticulitis. This e x p e r i e n c e stimulated o u r review o f Lahey Clinic patients with diverticulitis in w h o m colonic Crohn's disease was not discovered until o p e r a t i o n for a second stage resection or a later p r e s u m e d recurrence o f diverticulitis. Hence, this series represents a g r o u p o f patients with Crohn's colitis masquerading as clinical diverticulitis. Since Crohn's disease in these patients did not become a p p a r e n t until middle life or later, we have chosen the descriptive term "late onset Crohn's disease" for this g r o u p o f patients. 2

Materials and M e t h o d s

Twenty-five patients treated at the Lahey Clinic from 1957 t h r o u g h 1978 f o r m the basis o f this study. All 25 patients eventually p r o v e d to have c o m b i n e d diverticulitis and Crohn's disease. An initial diagnosis o f surgical diverticulitis was made on clinical g r o u n d s in each patient. Findings included abdominal pain and tenderness, fever, leukocytosis, pelvic mass, or signs o f peritoneal irritation. Operative impression in all 25 patients was acute diverticulitis. Histopathologic d o c u m e n t a t i o n o f diverticulitis was obtained on all patients whose original abdominal operation included colonic resection.

* Read at the meeting of the American Society of Colon and Rectal Surgeons, Atlanta, Georgia, June 10 to 14, 1979. ? Current address: 2432 Parkwood Drive, Brunswick, Georgia 31520. Address reprint requests to Dr. Corman: Section of Colon and Rectal Surgery, Lahey Clinic Foundation, 605 Commonwealth Avenue, Boston, Massachusetts 02215.

Each patient's history was followed until the patient died or until 1979 and included t e l e p h o n e contact for patients for w h o m c u r r e n t follow-up data had not been d o c u m e n t e d . Patient records were e x a m i n e d for evidence that might have suggested the coexistence of C r o h n ' s d i s e a s e a n d d i v e r t i c u l i t i s b e f o r e hist o p a t h o l o g i c c o n f i r m a t i o n was available. In this context, the existence o f a n o r e c t a l disease, rectal bleeding, a b n o r m a l sigmoidoscopy, a b d o m i n a l or extra-abdominal fistulas, multiple a b d o m i n a l operations, and extracolonic manifestations o f Crohn's disease was d o c u m e n t e d in addition to c o n v e n t i o n a l signs and s y m p t o m s . Results were i n t e r p r e t e d in terms o f the o c c u r r e n c e o f these heralding features of Crohn's disease and the clinical course o f these patients with diverticulitis. In many instances the diagnosis of C r o h n ' s colitis was suspected but u n p r o v e d until a subsequent resection p r o v i d e d histopathologic p r o o f o f c o m b i n e d diverticulitis and Crohn's disease. Once the diagnosis of coexistent C r o h n ' s disease and diverticulitis for a given patient was p r o v e d histopathologically, the term " c o m b i n e d disease" was used. Since a threestage p r o c e d u r e is sometimes p e r f o r m e d for patients with p e r f o r a t e d diverticulitis, the p e r f o r m a n c e o f three or m o r e abdominal operations without permanent relief o f symptoms was c o n s i d e r e d especially significant. Because the manifestations o f Crohn's colitis in these patients were diverse, m a n y o f their operations were such as to resist precise c o m p a r i s o n with each other. For this reason, categories o f operative proced u r e s w e r e u s e d to d e s c r i b e t h e i r p r o c e d u r e s . Categories for initial operation included bowel resection with a stoma, bowel resection without a stoma, and decompressive stoma without resection. Categories o f p r o c e d u r e s for the most recent operation included resection with or without a stoma and proctocolectomy with requisite proximal stoma. T h e

0012-3706/79/1100/0524/$00.80 9 American Society of Colon and Rectal Surgeons 524

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CROHN'S DISEASE WITH DIVERTICULITIS

most recent operation was t e r m e d "definitive," since it r e p r e s e n t e d the last operative p r o c e d u r e a t t e m p t e d in o r d e r to provide p e r m a n e n t relief o f symptoms. Results for both categories o f o p e r a t i o n were expressed in terms o f success or failure of the operation to control the disease and in terms of the need for yet a n o t h e r later abdominal operation. Results

T h e 15 women and 10 men studied in this series had initial abdominal symptoms in middle age or later. Patients' ages r a n g e d f r o m 39 to 74 years; m e a n age for the entire g r o u p was 57 years (women, 60 years; men, 52 years). Initial symptoms and signs were usually compatible with the diagnosis o f diverticulitis and almost always included fever, pain, and abdominal tenderness. Abdominal, perianal, or perineal f i s t u l a s - - c o m m o n elements of the combined d i s e a s e - - w e r e rarely present as features of the initial illness. However, a history of previous anal or perianal disease was s o m e t i m e s o b t a i n e d . O p e r a t i v e summaries o f initial and second-stage abdominal operations frequently expressed unusual technical difficulty or confused intraoperative findings. T h e most c o m m o n initial operative p r o c e d u r e in these patients was proximal colonic diversion, often p e r f o r m e d without resection (Table 1). Hence, in the absence o f a resected specimen for histopathology in these patients, diagnosis o f diverticulitis was made on the basis of clinical findings and on macroscopic findings at operation. In patients who had colonic resection, the histopathologic diagnosis o f "simple" diverticulitis was c o n f i r m e d in all resected specimens. However, five o f the nine patients who had initial colonic resection for diverticulitis required at least one additional resection for this disease at a later date. T h r e e - s t a g e resection for acute diverticulitis was a c o m m o n surgical p r e f e r e n c e d u r i n g the early years o f this study; therefore, it was not unusual for such pa-

525

tients to u n d e r g o a second operative p r o c e d u r e for resection if the first o p e r a t i o n had been diversion. While ultimate quiescence o f sigmoid disease is comm o n in patients after colonic diversion for diverticulitis, colostomy was followed by persistence o f sigmoid disease in the 16 patients who had diversion without resection. This was manifest by r e c u r r e n t pelvic sepsis, new or r e c u r r e n t fistulas, or rectal bleeding. Seven patients had p r i m a r y resection and anastomosis without diversion as an initial operative procedure. T w o o f these patients are well more than two years after resection. T w o o t h e r patients have continuing disease without requiring f u r t h e r operation two and five years after operation. In the r e m a i n i n g three patients, f u r t h e r o p e r a t i o n was r e q u i r e d between two and f o u r years later. T h e third operative g r o u p includes two patients in w h o m primary resection combined with diversion was p e r f o r m e d as an initial p r o c e d u r e . Both o f these patients r e q u i r e d a subsequent abdominal o p e r a t i o n 1 year and 13 years later. Symptoms and signs o f r e c u r r e n t illness were similar to those present when the patient was first seen, although fistulas were m o r e c o m p l e x and general medical condition often m o r e desperate. In patients who ultimately p r o v e d to have c o m b i n e d Crohn's disease and diverticulitis, there was often a history o f smoldering illness, contrasting with the m o r e episodic character o f diverticulitis alone. In retrospect only, barium e n e m a examination was sometimes suggestive o f Crohn's disease, but the impression was rarely suggested in radiographic reports. I n t r a m u r a l tracking of contrast material, increased retrorectal space, and r e c t o s i g m o i d stenosis were suggestive radiographic features f o u n d in some patients. Table 2 lists associated clinical findings in these groups o f patients. Anorectal disease was c o m m o n (76 per cent) manifesting fissure, fistula, anal ulceration, nodularity, tenderness, narrowing, or e d e m a t o u s skin tags. A history o f rectal bleeding was also f r e q u e n t (52 per cent),

TaBCE 1. Results of Initial Operation

No Further Operation

Procedure Diversion alone, no resection Resection and anastomosis, no diversion Resection with proxirnaI diversion

Number of Patients 16 7 2

Improved

Distal Disease Continues

Subsequent Operation: Distal Disease Continues

-2 --

-2 --

16 3 2

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B E R M A N , E T AL.

TABLE 2.

Associated Clinical Findings N u m b e r of Patients

Per C e n t

Anal or perianal disease

19

76

Rectal bleeding

13

52

A b n o r m a l sigmoidoscopy

19

90*

Persistent disease despite diversion

18

72

T h r e e or m o r e o p e r a t i o n s

17

68

Nov.-Dec. 1979

postoperative), all patients in this group are well between three and six years after operation. The most recent proctocolectomy was performed principally for control of lower extremity pyoderma of several months' duration, which was refractory to medical management. Within one week of proctocolectomy, this patient's pretibial ulcerations were healing. Several weeks of serial sectioning of the colonic specimen were required to confirm with certainty a diagnosis of combined Crohn's colitis and diverticulitis.

* T w e n t y - o n e patients e x a m i n e d .

Discussion

and when taken in combination with anorectal disease comprised 88 per cent of the total patient group. Sigmoidoscopy revealed abnormal findings in 90 per cent of 21 patients examined. Three or more abdominal operations were required for persistent or recurrent disease in 17 patients (68 per cent). Even with proximal diversion, distal disease continued in 72 per cent of our patients. The most recent surgical procedure for patients is described in Table 3. Seven of these patients had coIonic resection and primary anastomosis as a most recent "definitive" operative procedure. Two of this group have done well without further disease more than two years after operation. A third patient, seven years after resection, has had only occasional minimal rectal bleeding. Three of these patients have had continued distal disease (rectosigmoid colon), and one patient died from pelvic sepsis. A second operative group of 10 patients had resection and anastomosis with a protective proximal stoma as a most recent definitive surgical procedure. Two of these patients have done well for three and four years respectively after resection, but all of the eight remaining patients with resection and proximal stoma have done poorly; three of these eight have died from pelvic sepsis. The third operative group contains eight patients who had proctocolectomy for defi:fitive surgical therapy. All of this group have done well up to eight years after operation. If the two most recent patients who had proctocolectomies are excluded (each less than six months TABLE 3.

Resection a n d anastomosis, no p r o x i m a l diversion Resection with ileostomy or colostomy* Resection with p r o c t e c t o m y * Colostomy alone in o n e patient.

Crohn's disease of late onset, by definition, is more common in patients beyond middle age and, with advancing years, appears to gravitate to the colon. 2,a In some series, nearly all patients p r e s e n t i n g with Crohn's disease after age 60 have large bowel involvement. 4 Unlike Crohn's disease in younger patients, Crohn's disease in the elderly is less likely to involve the small intestine and perhaps more likely to respond to surgical extirpation, s'6 When Crohn's disease occurs in the setting of colonic diverticula, it may masquerade as clinical diverticulitis. Meyers et al. 2 suggested that diverticulitis and peridiverticulitis may result from infection of an aphthous ulcer, which may invade the mucosa of diverticula. In this series, all patients had an initial clinical diagnosis of diverticulitis, including nine patients from whom a resected specimen proved diverticulitis. Therefore, our series suggests that diverticular disease often precedes Crohn's disease. However, the point at which C r o h n ' s colitis becomes histopathologically evident is not clear, for we have seen other patients who had resection for Crohn's disease preceding later resection which showed both diverticulitis and Crohn's colitis. Hence, the answer to the question as to whether diverticulitis is precipitated by or simply is associated with Crohn's disease remains less than conclusive. The distinction between the two diseases is relatively important since medical and surgical management differs. Traditional medical management of acute diverticulitis includes restriction of oral intake,

Results of Most Recent Operation Number of Patients

Improved, No Distal Disease

Distal Disease Continues

Septic Death

7

3

3

1

10

2

5

3

8

8

--

--

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intravenous feedings, and parenteral antibiotics. If Crohn's disease could be confirmed, a cautious trial o f o t h e r modalities, such as intravenous hyperalimentation, azulfidine, or corticosteroids, could be considered in selected patients before a surgical p r o c e d u r e . Likewise, if Crohn's colitis is known, a more extensive surgical p r o c e d u r e may be w a r r a n t e d for r e c u r r e n t disease r a t h e r than risk the possibility o f pelvic sepsis or complications o f long-term corticosteroid therapy. T h e division in this series o f septic deaths with multiple p r o c e d u r e s versus healthy patients with proctocolectomy is remarkable. Clearly, r e c u r r e n t Crohn's colitis is not cancerous, but it is also not benign. In terms o f features that may be used to differentiate between the two diseases, the following highlights may be considered (Table 4). While the age spectrum of patients with Crohn's colitis and diverticulitis is similar, m o r e women in o u r series were affected with c o m b i n e d disease than is customary for diverticulitis alone. Meyers et al. 2 also made this observation. T h e most reliable hallmarks of Crohn's disease present in these patients were anorectal disease, rectal bleeding, and fistulas. L o c k h a r t - M u m m e r y and Morson r stated that anal disease may p r e c e d e the onset o f colonic Crohn's disease by months to years. T h e r e f o r e , a history of anorectal involvement may be equally as i m p o r t a n t as obvious ongoing anorectal disease. 8'9 I n s p e c t i o n o f the anal area may show e d e m a t o u s skin tags, ulcers, fissures, or fistulas. Even gentle digital rectal examination will often be painful for these patients with evidence of nodularity or narrowing o f the anal canal and blood on the e x a m i n i n g f i n g e r . S i g m o i d o s c o p i c f i n d i n g s are v a r i a b l e in Crohn's colitis, but sigmoidoscopy is more likely to reveal abnormalities with Crohn's colitis than with diverticulitis. In o u r series, 90 per cent o f patients e x a m i n e d had a b n o r m a l sigmoidoscopic findings, which included mocosal granularity, friability or inflammation, obliteration of vascular pattern, and pus in the rectosigmoid lumen. Hence, even acute clinical illness should not p r e c l u d e gentle sigmoidoscopic examination by s o m e o n e with sufficient e x p e r i e n c e to gauge both the extent o f mucosal involvement and the safety o f passage o f the instrument. Rectal bleeding was a f r e q u e n t o c c u r r e n c e in o u r series. Greenstein and associates ~~ related a 45 per cent incidence o f blood in the stool o f patients with colonic Crohn's disease in contrast to a much lower incidence of bleeding with Crohn's disease of the small bowel. Schmidt and co-workers ~I related an inci'dence o f 77 per cent rectal bleeding with c o m b i n e d Crohn's disease and diverticulitis c o m p a r e d to 20 per cent with diverticulitis alone. In o u r series, combined Crohn's disease and diverticulitis was accompanied by

TABLE 4.

Clinical Highlights

History Rectal bleeding C u r r e n t or previous anorectal disease Clinical recurrences with fistulas Multiple abdominal operations Confused intraoperative findings Unusual technical difficulties at operation Oral, hepatic, cutaneous, or joint disease Physical examination O n e or more abdominal incisions Abdominal, flank, rectovaginal, or perineal fistula Anal/perianal edema, fissure, fistula, or abscess T e n d e r rectal examination Blood on examining finger Abnormal findings on sigmoidoscopy Signs of oral, cutaneous, or joint disease Laboratory A b n o r m a l liver chemistries Diverticulitis or diverticulosis on barium examination Radiographic evidence o f Crohn's disease Clinical course Distal disease continuing or r e c u r r e n t Persistent or recurrent pelvic sepsis Weight loss and anemia Multiple abdominal operations

an incidence o f obvious bleeding o f 52 per cent, alt h o u g h bleeding was rarely massive. Eighty-eight per cent o f patients with c o m b i n e d Crohn's disease and diverticulitis had rectal bleeding or anal disease or both. Fistulas o t h e r than those associated with anal or perianal disease may occur in a wide variety o f locations. Colcock and S t a h m a n n 12 r e p o r t e d mostly colovesical and colocutaneous fistulas in 64 patients with diverticular disease; only 17 had colovaginal fistulas. Perineal, low rectovaginal, flank, and thigh fistulas are less likely to be associated with diverticulitis, and their presence makes combined Crohn's disease and diverticulitis suspect. However, fistulas per se are not diagnostic o f Crohn's disease. T h u s , it is unreasonable to attribute instances o f clinical deterioration after colonic resection to C r o h n ' s colitis, for a surgical complication remains the most likely source o f fistula in the early postoperative period. While all patients who died in o u r series had c o m b i n e d diverticulitis and Crohn's disease with both sepsis and fistulas, a retrospective analysis o f specimens f r o m 10 o t h e r patients who died with a diagnosis of fistulas complicating diverticulitis showed no evidence o f Crohn's disease whatsoever. T h e s e observations serve to emphasize that indications for r e o p e r a t i o n in instances o f early p o s t o p e r a t i v e fistulization should not be clouded by considerations r e g a r d i n g the possibility o f unsuspected Crohn's colitis.

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BERMAN, ET AL.

-J CLINICAL DIVERTICULITIS

MILD OR UNCOMPLICATED

I

I

RESECTION (I or 2 stages) PATH = DIVERTICULITIS

MEDICAL MANAGEMENT

I

~-_

4, CLINICAL RECOVERY

I SUSPECT CROHN check o.r pothology

diagnostic workup

k

MEDICAL MANAGEMENT

i

"v I

CLINICAL RECOVERY

UNIMPROVED

MODERATE TO SEVER--~ ANORECTAL DISEASE I

MINIMAL OR NO t ANORECTAL DISEASE

J

I

4, biopsy or resec ion

B U T UNPROVEN

CROHN'S PROVEN biopsy

]

J STAGED RESECTION

r

PERSISTENT OR RECURRENT DISEASE

I

,•

I

RECOVERY

?

v PROCTOCOLECTOMY

SEGMENTAL RESECTION t DIVERSION

FIc. l. Schema for possible patient management after colonic resection for diverticulitis. Decisions regarding proctocolectomy

are based on extent of anorectal disease and the number and severity of recurrences. O t h e r features in this series also a p p e a r to be useful irl differentiating combined diverticulitis and Crohn's disease from diverticulitis. T h e most obvious is the presence o f extracolonic manifestations, such as arthritis, stomatitis, and p y o d e r m a , which are not associated with diverticulitis in the absence o f Crohn's disease? a A s m o l d e r i n g illness, perhaps with anemia and weight loss, also favors combined disease as opposed to the m o r e episodic character o f r e c u r r e n t diverticulitis. Clinical diverticulitis with narrowing or diverticulosis on radiographic study may also favor a diagnosis of c o m b i n e d disease. Unusual technical difficulty with resection was a p r o m i n e n t feature o f o u r series, and the operative dictations often reflected the surgeon's frustration even in the first operative procedure. It follows that patients with more than one resection for diverticulitis should immediately be suspect for c o m b i n e d disease.

Dis. Col. & Rect.

Nov.-Dec. 1979

O n e o f the most consistent features o f this series is the f r e q u e n t failure o f distal rectosigmoid disease to r e s p o n d to p r o x i m a l diversion either with o r without r e s e c t i o n . T h o m p s o n I4 n o t e d p e r s i s t e n t active C r o h n ' s disease in the bypassed rectum, and o u r series reflects a similar p h e n o m e n o n . C o l o s t o m y alone is now c o n s i d e r e d suboptimal for early mana g e m e n t o f p e r f o r a t e d diverticulitis, and two-stage resection with extirpation o f the disease is generally p r e f e r r e d as a first o p e r a t i v e p r o c e d u r e . In o u r series, distal disease rarely respected proximal diversion with or without resection, and distal persistence or r e c u r r e n c e was c o m m o n (72 per cent). T h e unif o r m success o f proctocolectomy in o u r series und o u b t e d l y reflects e l i m i n a t i o n o f the u n d e r l y i n g pathology. A reasonable a p p r o a c h to the problem o f r e c u r r e n t disease r e q u i r i n g s u r g e r y is expressed in Figure 1. M a n a g e m e n t of.the initial episode of a p p a r e n t diverticulitis should be along conventional lines: restriction o f oral intake, administration o f intravenous fluids and antibiotics, a n d f r e q u e n t e x a m i n a t i o n by the same observer. T h o s e patients who do not i m p r o v e or b e c o m e worse may have resection in o n e or two stages. If the p r o c e d u r e is p e r f o r m e d without satisfactory bowel p r e p a r a t i o n or if peritoneal contamination is present, resection with or without p r i m a r y anastomosis but with proximal diversion is p r e f e r r e d . Early r e c u r r e n c e or fistula f o r m a t i o n after resection is first viewed as a possible complication o f the surgical p r o c e d u r e . H o w e v e r , c o n t i n u e d rectal bleeding, later fistulas, or late pelvic sepsis should be r e g a r d e d with suspicion for possible combined C r o h n ' s disease and diverticulitis, especially if o t h e r hallmarks o f C r o h n ' s disease are p r e s e n t . I f the patient is not acutely ill, radiographic contrast studies may be perf o r m e d to ascertain f u r t h e r intestinal involvement. In s u b a c u t e o r c h r o n i c illness, s i g m o i d o s c o p y o r colonoscopy may a f f o r d an o p p o r t u n i t y for visualization and for biopsy that may prove the diagnosis. I f the presentation is acute, it may be necessary to rely principally on clinical findings and gentle sigmoidoscopic examination. In some patients who are not severely ill, a p p a r e n t r e c u r r e n c e o f clinical diverticulitis with the hallmarks o f Crohn's disease may justify a trial o f azulfidine, even without absolute c o n f i r m a t i o n o f Crohn's colitis. If peritonitis and sepsis are not present, corticosteroid t h e r a p y may also be considered. Failure to i m p r o v e or clinical d e t e r i o r a t i o n would necessitate a surgical procedure. Decisions r e g a r d i n g the optimal o p e r a t i o n for rec u r r e n t or persistent illness when Crohn's disease is suspected may t h e n be based u p o n anorectal findings.

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DISEASE WITH

T h u s , i f s e v e r e a n o r e c t a l d i s e a s e is p r e s e n t a n d C r o h n ' s d i s e a s e is p r o v e d , p r o c t o c o l e c t o m y is w a r ranted. Without such proof, diversion with or without r e s e c t i o n m a y allow a n o p p o r t u n i t y to p r o v i d e clinical improvement while a definite diagnosis may be establ i s h e d at a l a t e r t i m e . W h e n still a n o t h e r s u r g i c a l p r o c e d u r e is r e q u i r e d a n d s e v e r e a n o r e c t a l d i s e a s e is p r e s e n t , p r o c t o c o l e c t o m y is p r o b a b l y w a r r a n t e d e v e n without an absolute diagnosis of Crohn's disease.

Summary and Conclusions T w e n t y - f i v e p a t i e n t s h a d C r o h n ' s d i s e a s e in a coIonic s p e c i m e n r e s e c t e d f o r p r e s u m e d d i v e r t i c u l i t i s . A s y n d r o m e o f c o m b i n e d d i v e r t i c u l i t i s a n d C r o h n ' s colitis is p r e s e n t e d , w h i c h is h e r a l d e d by a n o r e c t a l dise a s e , r e c t a l b l e e d i n g , a n d f i s t u l a s . T h e i l l n e s s is characterized by multiple operations, failure of divers i o n a r y p r o c e d u r e s to c o n t r o l d i s t a l disease, a n d a h i g h i n c i d e n c e o f l e t h a l pelvic sepsis. Results o f t h e s e p a t i e n t s ' s t u d i e s s u g g e s t t h a t late o n s e t C r o h n ' s colitis s h o u l d b e c o n s i d e r e d w h e n clinical d i v e r t i c u l i t i s is present associated with anorectal disease (past or p r e s e n t ) , r e c t a l b l e e d i n g , fistulas, o r e x c e p t i o n a l difficulty with an initial resection for diverticulitis. Patients with persistence of disease after colonic resection, d i s t a l r e c u r r e n c e a f t e r d i v e r s i o n , o r l a t e fistulization after resection for diverticulitis should be c o n s i d e r e d to h a v e C r o h n ' s c o l i t i s u n t i l p r o v e d otherwise. Also, patients requiring multiple resections f o r clinical d i v e r t i c u l i t i s a r e also s t r o n g l y s u s p e c t f o r Crol-m's colitis. W h e n s i g n i f i c a n t a n o r e c t a l d i s e a s e is p r e s e n t a n d C r o h n ' s colitis is e i t h e r p r o v e d o r suspected, proctocolectomy may be warranted.

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Acknowledgment The authors wish to express their gratitude to Mrs. Marybeth Oster, ART, for her efforts in data collection and patient follow-up.

References 1. Leigh JE, Judd ES, Waugh JM: Diverticulitis of the colon: Recurrence after apparently adequate segmental resection. AmJ Surg 103: 51, 1962 2. Meyers MA, Alonso DR, Morson BC, et ah Pathogenesis of diverticulitis complicating granulomatous colitis. Gastroenterology 74: 24, 1978 3. Small WP, Smith AN: Fistula and conditions associated with diverticular disease of the colon. Clin Gastroenterol 4: 171, 1975 4. Alexander-Williams J: Late-onset Crohn's disease. The Management of Crohn's Disease. Edited by IT Weterman, AS Pena, CC Booth. Amsterdam, Excerpta Medica, 1976, p 43 5. De Dombal FT, Burton I, Goligher JC: Recurrence of Crohn's disease after primary excisional surgery. Gut 12: 519, 1971 6. Nugent FW, Veidenheimer MC, Meissner WA, et al: Prognosis after colonic resection for Crohn's disease of the colon. Gastroenterology 65: 398, 1973 7. Lockhart-Mummery HE, Morson BC: Crohn's disease of the large intestine. Gut 5: 493, 1964 8. Homan WP, Tang C, Thorbjarnarson B: Anal lesions complicating Crohn disease. Arch Surg 111: 1333, 1976 9. Marshak RH, Janowitz HD, Present DH: Granulomatous colitis in association with diverticula. N Engl J Med 283: 1080, 1970 10. Greenstein AJ, Kark AE, Dreiling DA: Crohn's disease of the colon. II. Controversial aspects of hemorrhage, anemia and rectal involvement in granulomatous disease involving the colon. Am J Gastroenterol 63: 40, 1975 11. Schmidt GT, Lennard-Jones JE, Morson BC, et ah Crohn's disease of the colon and its distinction from diverticulitis. Gut 9: 7, 1968 12. Colcock BP, Stahmann FD: Fistulas complicating diverticular disease of the sigmoid colon. Ann Surg 175: 838, 1972 13. Lennard-Jones JE: Differentiation between Crohn's disease, ulcerative colitis and diverticulitis. Clin Gastroenterol 1: 367, 1972 14. Thompson H: Activity of Crohn's disease in the bypassed rectum. The Management of Crohn's Disease. Edited by IT Weterman, AS Pena, CC Booth. Amsterdam, Excerpta Medica, 1976, p 26