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Bleeding in colonic diverticulitis
Bleeding in Colonic Diverticulitis JACK E . MOBLEY, M .D ., MALCOLM
B.
DOCKERTY, M .D . AND JOHN
M.
WAUGH, M .D .,
Rochester, Minnesota
From the Sections of Surgery and Surgical Pathology, Mayo Clinic and Mayo Foundation, Rochester, Minnesota . The Mayo Foundation is a part of the Graduate School of the University of Minnesota .
to ulceration within a diverticulum, and in a few instances such lesions have been seen . Actually, detailed pathologic studies of sufficient magnitude to allow determination of the frequency of such findings have not been published . McGrath [7], in rgr2, noted mucosal ulceration in eleven of twenty-seven surgical specimens, but he made no attempt to correlate this alteration with clinical findings. d e Quen'ain [2] described a "hemorrhagic form" of diverticulitis, about which he made this statement : "The patient is distressed, at times, by fairly severe intestinal hemorrhage, which clearly arises from ulcerative erosion of small vessels in the diverticulum ." It is impossible to determine whether or not de Quervain actually saw such ulceration, because pathologic studies were not included in his article . Synnott 112] stated that bleeding in diverticulitis originated in "eroding ulcerations of the mucosa lining the diverticulum or in small polyps in the diverticular area and not in the mucosa of the colon itself ." Again, corroborative pathologic studies were not presented . That ulceration within diverticula does account for some instances of bleeding was proved by Kocour [q], who reported a death caused by hemorrhage from an eroded artery in a diverticulum . Smith [it] reported the sigmoidoscopic visualization of several bleeding diverticula in a patient who had massive gastrointestinal hemorrhage . Young and Howorth [14] reported a case of diverticulitis and bleeding in which the surgical specimen contained numerous diverticula, several of which were inverted into the intestinal lumen . Ulceration was present on the mucosa of one of these inverted diverticula and this was considered to be the source of hemorrhage . These observers were unable to find any mention of inversion of diverticula in the literature . It appeared to them that an inverted diverticu-
the beginning of this century, diverticulitis of the colon has become a well recognized clinical and pathologic entity . More recently, its medical and surgical implications have been studied thoroughly and attempts have been made to establish the proper principles of management of this disease and its complications . Consequently, rather extensive information is available regarding the clinical and pathologic manifestations of acute diverticulitis, diverticulitis with perforation, diverticulitis with abscesses and diverticulitis with fistulas. Although hemorrhage in association with diverticulitis also has received considerable attention, information about this particular complication, especially regarding its pathogenesis, is not so nearly complete as might be desirable . Throughout the past fifty years, authorities on this subject repeatedly have warned physicians to search diligently for causes other than diverticulitis when rectal bleeding occurs . This is still sound advice despite the fact that bleeding can occur from diverticulitis alone . The frequency with which such bleeding occurs in cases of diverticulitis has been reported to be from 3 to 47 per cent, but the majority of studies report a frequency of ro to 30 per cent . The bleeding may be of any magnitude but is usually moderate in amount . The pathogenesis of bleeding directly attributable to diverticulitis has not been extensively investigated, although Neer [8], McGrath [7], Kocour [f], de Quervain [21, Young and Howorth [741, Lahey [6], Hoar and Bernhard [4], and Quinn and Ochsner [9] have made significant contributions . The bleeding usually has been attributed to ulceration of the colonic wall or INCE
American Journal
of
Surgery, V-1-me 94,
July, 1957
44
Bleeding in Colonic Diverticulitis Ium might bleed just as a polyp does when its surface becomes ulcerated . They pointed out that large vessels frequently are present about the bases of diverticula that might he the source of hemorrhage . Rosser [io] and Boyd [r] suggested that bleeding may arise from granulation tissue in diverticula that are the site of inflammation . Hickey 13] reported an unusual case in which an abscess had perforated into the inferior epigastric artery, with severe hemorrhage . Hoar and Bernhard [4] recently contributed valuable information regarding the pathologic findings in diverticulitis with bleeding . They found that forty-two of iii patients with diverticulitis had rectal bleeding . They examined pathologic specimens from three of these patients . In one specimen, four of five diverticula sectioned showed engorged granulation tissue replacing part of the mucosa . Ulceration was present in several of the diverticula in another specimen . The source of bleeding was not discovered in their third case . Of sixty-eight patients with divcrticulitis and diverticulosis reported by Noer [8], twenty had bleeding as a presenting or major symptom . Six of these patients underwent resection and specimens were examined pathologically in all six ; ulceration was found in one of the specimens . Bleeding from diverticulitis may occur in the presence of one of the other complications of the disease, or it may be the only complication present . The amount of blood lost is usually small or moderate, but in a significant number of cases it has been excessive, even to the point of being termed "exsanguinating ." Hoar and Bernhard [4] stated that most of the patients who have massive bleeding are more than sixty years of age and they frequently have arterial hypertension . It is often difficult to establish a clinical diagnosis of "bleeding diverticulitis ." Quinn and Ochsner [9] gave the following criteria that, when fulfilled, justify the assumption that the bleeding is from diverticulosis or diverticulitis : passage of gross blood per rectum ; evidence of diverticulitis or diverticulosis after use of a barium enema ; absence of other intrinsic lesions on rectal or proctoscopic examination ; roentgenographic studies demonstrating the stomach and small intestine to be normal . Thus, it is apparent that the diagnosis is often by exclusion .
The management of this complication of diverticulitis usually has been conservative, consisting of measures designed to put the intestine at rest, the administration of antibiotics and whole blood when indicated, and general supportive therapy . For the most part, this regimen has been adequate and surgical intervention has been used in the past only in those cases in which other indications for operation were present or in which the bleeding could not be controlled by medical means . Recently, however, surgical resection of the affected portion of colon has been used more extensively in the treatment of recurrent, persistent or severe hemorrhage . The present study was undertaken in an effort to correlate the pathologic features and the clinical manifestations of this complication of diverticulitis of the colon in the hope that such a correlation might contribute to better understanding and management of this disease . PRESENT STUDY
The diagnosis of diverticulitis of the colon was recorded for 1,970 patients at the Mayo Clinic from 1940 to 1954, inclusive . Of these patients, 145 (7 .4 per cent) gave histories of having passed blood by rectum for which no cause other than the diverticulitis could he found . Pathologic specimens preserved in formalin were available for examination in thirty-two of these 145 patients who had rectal bleeding . Thirty of these specimens were obtained during surgical resection of the affected colonic segments, whereas two specimens were obtained at necropsy . The clinical records of these thirty-two patients were examined for pertinent data relating to age, sex, symptoms, physical and laboratory findings, treatment, clinical course and follow-up studies . The findings at operation or necropsy were noted . The specimens were studied grossly with special reference to the appearance and thickness of the colonic mucosa, the presence or absence of ulceration, the diameter of the intestinal lumen, the thickness of the colonic wall, the presence or absence of zones of hemorrhage, the number of diverticula present, and the extent of diverticulitis . Multiple gross cross sections of the specimens were made for further examination of the areas of diverticulitis . Particular attention was paid to those regions in which extravasation of blood was 45
Mobley, Dockerty and Waugh evident. Blocks of tissue for microscopic study were taken from any obvious regions of ulceration or hemorrhage . Additional blocks of tissue were taken from any suspicious portions encountered during examination . Sections for microscopic examination were prepared and stained with hematoxylin and eosin in the usual manner . The original sections were available in ten of the thirty-two patients . All sections were studied to determine the characteristic picture present, and a search was made for any features that might account for the clinical bleeding . Six specimens of colon removed surgically for diverticulitis or one of its complications other than bleeding were picked at random for control specimens . These were examined in exactly the same manner as were the aforementioned thirty-two specimens .
one of the major complaints in fifteen patients . The most frequently noted physical findings and the number of cases in which each finding was encountered were abdominal tenderness (fifteen), extrarectal mass (nine), mass in the left lower abdominal quadrant (six) and intrarectal mass (two) . Although most of the patients had physical findings suggestive of diverticulitis, the results of examinations were completely negative in seven patients (22 per cent) . Results of routine laboratory studies were within normal limits except for the patient who had massive bleeding and in whom the value for hemoglobin was less than to gm . per loo ml . of blood . Proctoscopic examinations were performed on twenty-nine patients . Diverticula were seen in seven patients, and the findings were suggestive, but not diagnostic, of diverticulitis in nine others . Bleeding zones were seen in the intestinal mucosa in two patients . In one patient, an erroneous diagnosis of carcinoma was made . Entirely negative results of proctoscopic examination were recorded for seven patients . The three remaining patients had pathologic proctoscopic findings unrelated to the rectal bleeding . Roentgenologic examinations of the colon were done on thirty of the thirty-two patients . A definite diagnosis of diverticulitis was made in eighteen, and this diagnosis was suggested in four others . In the remaining eight patients, the radiologist considered a question of the presence of a neoplasm of the colon, but a definite roentgenologic diagnosis of carcinoma was reported in only one instance. Surgical exploration was performed on thirty-one of the thirty-two patients . Although rectal bleeding was frequently a major consideration in the decision to perform laparotomy, in only one patient was the problem of bleeding the sole surgical indication . The possibility of the presence of a malignant lesion undoubtedly influenced the decision to operate in many of these patients. Other indications were the existence of obstruction, the presence of an abdominal mass, and pronounced severity, persistence or recurrence of the symptoms of acute diverticulitis . Five different types of operative procedures were performed on the thirty-one patients just mentioned . Eleven underwent exteriorization procedures in which the affected loop of intes-
CLINICAL FINDINGS
Nineteen of the patients were men and thirteen were women . The range of age was from twenty-six to seventy-seven years, but only one patient was under forty . Five were in the fifth decade of life, thirteen were in the sixth decade and ten were in the seventh decade . Three patients were more than seventy years of age . Gross blood had been passed from the rectum by all the patients . The bleeding was often intermittent, and the blood usually was bright red . Bleeding was mild in twelve patients, moderately severe in nineteen and severe in one . Hemorrhage was the symptom that led the patient to seek medical care in seven instances (22 per cent) ; bleeding was the only symptom noted in six of these instances . The duration of bleeding varied considerably . Seventeen of the patients had noted blood in the stools for less than three months, whereas five patients had experienced bleeding for three months or more but less than a year . Ten patients had noted bleeding for a year or more, three of this latter group having observed it for more than five years. Rectal bleeding was overshadowed by other symptoms in twenty-five cases . In order of frequency, these were abdominal pain, chills, fever, diarrhea, decreased caliber of stools, constipation, dysuria and weakness . Although the presenting complaint was one other than bleeding, hemorrhage was recorded as being 46
Bleeding in Colonic Diverticulitis tine was brought out to the skin and subsequently excised, with extraperitoneal closure of the resulting colonic stoma as a final step . Primary resection with end-to-end anastomosis was performed in ten cases . Six patients underwent three-stage resection in which transversostomy preceded resection and anastomosis of the colon, the colonic stoma being closed later as a third stage. Three patients underwent primary resection and anastomosis with concomitant transversostomy and subsequent closure of the stoma . One patient underwent transversostomv but died before further surgical procedures could be performed. Except for this patient, all those treated surgically did well in the immediate postoperative period . Thrombophlebitis of the deep veins of one lower extremity developed in one patient but responded well to treatment . A fistula developed at the site of closure of the colonic stoma in another patient but later closed spontaneously . Twenty-four of the surviving patients have been followed up postoperatively for periods up to ten years . What was described as an episode of "intestinal obstruction" developed in one patient several years after operation ; he was hospitalized elsewhere and recovered with conservative management . The other twentythree patients have had no further symptoms attributable to diverticulitis . As previously indicated, two patients died . One died of peritonitis and bronchopneumonia after transversostomy . The other patient, who had massive rectal bleeding two weeks prior to admission, died of myocardial infarction . PATHOLOGIC FINDINGS
The length of colon that was resected varied from to to 35 cm ., the average being between Ig and zo cm . The zone of diverticulitis was in the sigmoid colon in twenty-seven patients and in the descending colon in four . Multiple regions of involvement were scattered from the ascending colon to the sigmoid in one patient . The pathologic findings generally were typical of those usually found in diverticulitis . Almost without exception there was segmental involvement characterized by pronounced edema. of the pericolonic tissues, thickening of the muscular wall, engorgement of blood vessels and, in more than half of the specimens,
narrowing of the intestinal lumen . For the most part, the inflammatory process appeared to involve small numbers of diverticula, even though multiple uninvolved diverticula might be present in other portions of the intestine . Microscopically, the intestinal wall and pericolonic tissues were infiltrated with polymorphonuclear leukocytes and, to a lesser extent, with mononuclear cells . The tissues were edematous and increased fibrous tissue could be found in the older lesions . The muscular layers of the intestine were thickened in many instances, particularly in those specimens in which the lumen was narrowed . In half of the specimens the mucosa was in polypoid folds which were so striking at times that they gave the appearance of true polyps . Flowever, close inspection revealed the true nature of the changes . Because of our particular interest in bleeding, a careful search for any changes pertaining to this was made . Gross examination revealed definite ulceration of the colonic mucosa in three specimens . Nineteen of the specimens had discolored zones in the mucosa suggestive of hemorrhage . Early in the gross study it was found that many areas of hemorrhage could be discovered by inspection of the colonic walls and the pericolonic regions . This proved to be one of the best methods of locating tissues from which bleeding might have originated . In eleven specimens, diverticula could he traced into, and grossly appeared to constitute aa part of, these hemorrhagic regions . An ulcerated inverted diverticulum was present in one specimen . Microscopic studies disclosed ulceration of the surface colonic mucosa in five other specimens in addition to the aforementioned three specimens in which ulceration was visible grossly. Microscopically, these ulcerated zones proved to be typical inflammatory ulcers characterized by absence of surface epithelium, destruction of the submucosa, vascular engorgement and evidence of acute inflammation . (Fig . I .) The ulceration in each of these eight instances was considered sufficient to produce bleeding, and good evidence of such bleeding was demonstrated in one section . Ulceration of the mucosa buried deeply in one or more diverticula was demonstrated microscopically in ten specimens . The microscopic picture of these ulcers was the same as that found in ulceration affecting the regular 47
Mobley, Dockerty and Waugh somewhere in the affected intestine, which is usually the sigmoid colon . This is borne out by the findings in the present study . In more than half of the specimens ulceration was noted in the colon or within diverticula . Other writers [4,8], have seen such ulceration in the intestines of patients who have bled from diverticulitis . It is assumed that such ulceration arises as a direct result of inflammation . It is possible that the trauma of the fecal current may contribute to the ulceration, but it appears that edema, exudation and necrosis of tissue could cause the ulceration within diverticula and that in the intestinal mucosa as well . It is not difficult to understand that bleeding may occur from a zone of diverticulitis that becomes ulcerated, especially in view of the pronounced vascular engorgement occurring within tissues affected by diverticulitis . One might wonder why bleeding does not occur more frequently . It is likely that many regions of ulceration were missed in the present study, because the method of gross serial sectioning employed was somewhat inadequate at best . Microscopic serial sectioning could be expected to increase the positive findings to a figure much nearer roo per cent than that reported herein . As already noted, one of our specimens contained an ulcerated inverted diverticulum . The possibility of this rare condition should be emphasized because of the danger of mistaking such a lesion for a polyp at proctoscopic examination . Cauterization or biopsy under such circumstances could produce serious consequences . The frequency with which diverticula could be traced into zones of gross hemorrhage and the microscopic demonstration of ulceration in these regions proved to be among the most interesting aspects of the present study . This occurred eleven times, and the microscopic findings were positive in eight cases. This would appear to be of significance, and it is possible that close attention to the involved segments of colon removed surgically in patients with clinical bleeding might reveal the source of bleeding in many instances . It might be well to re-emphasize the fact that a neoplasm of the colon is the cause of bleeding from the rectum far more frequently than is diverticulitis . Welch and associates [13] estimated that carcinoma of the colon is the cause of rectal bleeding five times as frequently as is diverticulitis . The presence of diverticu-
Frc . i . Colonic wall in diverticulitis with bleeding, demonstrating ulceration of the colonic mucosa. Note depth of penetration and the inflammatory reaction . Hematoxylin and eosin stain, original magnification
X 18 .
mucosa . Completely disrupted diverticula were seen in some sections, while less extensive ulceration was present in other specimens . (Figs . 2 and 3 .) In two instances in which microscopic ulceration of the colonic mucosa was found, additional ulceration within diverticula was present . In eight of the eleven specimens in which diverticula could be traced into regions of gross hemorrhage, microscopic examination revealed ulceration of the walls of the diverticula into the surrounding inflammatory hemorrhagic tissues . The extent of vascular engorgement in the inflamed tissues left little doubt that these ulcerated zones might be the source of significant bleeding . Thus, the gross and microscopic findings disclosed that eighteen (g6 per cent) of these thirty-two patients had ulceration either of the colonic wall or within diverticula . Similar studies of the control group of six specimens disclosed little difference in the over-all pathologic picture between the two groups of specimens . Absent in the control group, however, was evidence of hemorrhage or areas that might serve as sources of hemorrhage . Gross ulceration of the mucosa was absent, and microscopic examination failed to reveal any ulceration of the colonic wall or within diverticula . COMMENTS
It appears reasonable to assume that the origin of the bleeding in patients who have diverticulitis of the colon is from ulceration 48
Bleeding in Colonic Diverticulitis
Fir . 2. (a) and (h), Two examples of ulceration within a diverticulum in diverticulitis with bleeding . Hematoxylin and eosin stains, original magnification X i6 .
Fir . 3 . (a), Diverticulum with ulceration in diverticulitis with bleeding . Hematoxylin and cosin stain, original magnification X i6. (h), Wall of diverticulum shown in (a) . Note ulceration and surrounding inflammatory reaction . Hematoxylin and rosin stain, original magnification X 170.
49
Mobley, Dockerty and Waugh litis does not give any assurance that a concomitant carcinoma is not present . The aforementioned total of 1,970 patients surveyed in the present study included ion patients who had simultaneous diverticulitis and carcinoma . Carcinoma of the colon has received emphasis as the principal disease to be differentiated from diverticulitis in patients who have rectal bleeding, and it is probably the most important one. However, other diseases of the anal canal and colon must be considered in dealing with these patients . External and internal hemorrhoids, fissures, adenomatous polyps and ulcerative colitis are all capable of causing rectal bleeding . In addition, lesions of the upper part of the gastrointestinal tract, such as peptic ulcer, gastric neoplasm, Meckel's diverticulum and neoplasms of the small intestine, may produce bleeding that is difficult to differentiate from colonic bleeding. All these conditions must be considered before a diagnosis of diverticulitis with bleeding is made . The differentiation of these conditions frequently cannot be made until the time of operation, and occasionally the correct diagnosis cannot be made even then . The bleeding from diverticulitis characteristically is associated with other symptoms of diverticulitis, and a history of intermittent attacks may be obtained . However, 1q per cent of our thirty-two patients had bleeding as the only symptom . The bleeding usually is small or moderate in amount, but instances of massive bleeding have been recorded, as occurred in one of the patients in this study . The bleeding was often recurrent or intermittent in character . One-third of the patients gave histories of recurrent attacks of bleeding for more than one year . The bleeding often is a relatively minor symptom in the clinical picture, and the major complaints are those more characteristic of diverticulitis, such as abdominal pain, chills, fever, dysuria and diarrhea . Although the physical findings usually associated with diverticulitis may be present, the general examination may not be helpful insofar as the differential diagnosis of rectal bleeding is concerned, and sometimes the results of physical examination may be entirely normal . Proctoscopic and roentgenologic examinations have proved valuable in the study of these patients. About half of the patients who underwent proctoscopic examinations had find-
ings either diagnostic of or suggestive of diverticulitis . A definite roentgenologic diagnosis of diverticulitis was made in 6o per cent of the patients so examined . As useful as these examinations may be, it must be remembered that they are not infallible and that the presence of diverticulitis does not exclude the possibility of other disease . The management of patients who have "bleeding diverticulitis" usually has been conservative in the past . Such management appears reasonable for patients in whom the diagnosis can be definitely established and who exhibit bleeding for the first time . However, recurrent hemorrhage is not infrequent, and it is often impossible to exclude the possibility of malignant lesions. In these instances, it would be wiser to employ surgical therapy . Bleeding rarely is the only indication for surgical intervention in these patients ; only one patient in the present study had bleeding as the sole surgical indication . Some other complication of diverticulitis or doubt as to the nature of the pathologic process usually dictates the surgical approach . Generally speaking, indications for laparotomy in diverticulitis have been, and are, increasing. Indications for operation in "bleeding diverticulitis" probably will follow the same pattern. The surgical procedures performed for the patients in this study were predominantly multiple-stage resections, which have proved to be an adequate method of management, particularly for the extremely ill patient . Because of improved operative technics, better anesthesia, use of chemotherapeutic and antibiotic agents, and more efficient preoperative and postoperative care, primary resection of the colon recently has been used more frequently . The role of primary resection may increase in scope as surgical technics advance, but some patients still will require multiple-stage operations because of debility, extensive local disease or technical factors . The surgical procedure necessary in a given case is probably best decided in the operating room, where the extent of the disease can be evaluated . The final results of surgical therapy in the present group of patients have been satisfactory, although it is difficult to draw any extensive conclusions from such a small group. One patient died after transversostomy, death being due to perforation of the colon and peritonitis . The other patients who have been adequately 50
Bleeding in Colonic Diverticulitis followed up have (lone well except for minor complications .
REFERENCES BOYD, J . T934-
T. Diverticulosis and diverticulitis . Texas J . Med ., 43 : 681-685, 1948 . DE QUERVAIN, F . Dvverticulosis and diverticulitis of the large intestine . Practitioner, i IS : 352-360,
SUMMARY AND CONCLUSIONS
Detailed pathologic, clinical and follow-up studies have been made on thirty-one patients who underwent surgical treatment at the Mayo Clinic for colonic diverticulitis associated with bleeding and on one patient who died from myocardial infarction two weeks after massive rectal bleeding accompanying diverticulitis . Hemorrhage is a proved complication of diverticulitis . Although it is relatively rare, it must be considered in the differential diagnosis of rectal bleeding . The bleeding arises from ulceration of the affected colonic wall or ulceration within one or more diverticula . The bleeding is usually small or moderate in amount, is frequently recurrent over long periods and is usually associated with other symptoms of diverticulitis . It is difficult to differentiate bleeding due to diverticulitis from that due to neoplasm, and both diseases may occur simultaneously. The physical findings in "bleeding diverticulitis" are not characteristic . Roentgenologic and proctoscopic examinations are helpful in establishing a diagnosis, but neither should he considered infallible . In patients with diverticulitis, the complication of hemorrhage can be treated conservatively in many instances, provided that no doubt exists concerning the diagnosis . Surgical resection of the affected colon is justified in patients who have recurrent or uncontrollable hemorrhage, in those in whom the presence of a neoplasm cannot be excluded and in those who have indications for operation other than hemorrhage.
1927 . . HICKEY, R . 3-4-5
C . Massive colonic bleeding secondary to diverticulitis . Gastroenterology, 26 : 754-757, 1954 .
C. S . and BERNHARD, W . F . Colonic bleeding and diverticular disease of the colon . Surg., Gynec. e+Obst ., 99 : ioi - 107, 1954 . KocouR, E . J . Divcrticulosis of the colon : its incidence in 7,000 consecutive autopsies with reference to its complications. Am . J . Surg., 37 :
HOAR,
433 -436, 1937
F . H. The advantages of an hepatic flexure Mikuliez type of defunctionalizing colostomy in the surgical treatment of diverticulitis . Label , Clin . Bull., 6 : 34 -37, 1 948 . MGGRATH, B . F . Intestinal diverticula : their etiology and pathogenesis ; with a review of twentyseven cases . Surg ., Gynec . er Obst., 15 : 429 444,
LAHEY,
7.
1912. 8 . NOER, R.
J . Hemorrhage as a complication of diverticulitis . Ann . Surg ., 141. 674-685 . 1955 9 . QUINN, W . C . and OcHSnnR, A . Bleeding as a complication of diverticulosis or diverticulitis of the colon. Am . Surgeon, 19 : 397 - 402, 195310 . RossER, C . Changing concepts concerning diverticulitis . J . Internat. Coll. Surgeons, 14 : 52-56, 1950 . II . SMITH, N . D .
Diverticulosis and diverticulitis : general consideration and sigmoidoscopic diagnosis . Am . J. Surg., 82 : 583-586, 1951 . cz. SY V VUTI', M . J . Diverticulitis . M . J. e- Rec ., 138 : 253 -257, 1933 . 13 . WELCH, C . F ., ALLEN, A . W . and DONALDSON, G . A . An appraisal of resection of the colon for diverticulitis of the sigmoid . Ann . Surg ., 138 : 332- 343-193314 . YOUNG, J . M . and HowoRTH, M . B ., JR. Massive
hemorrhage in diverticulosis : possible explanation of cause with presentation of case requiring surgical treatment . Ann . Sure ., 140 : 128-131,
51
B.
DOCKERTY, M .D . AND JOHN
M.
WAUGH, M .D .,
Rochester, Minnesota
From the Sections of Surgery and Surgical Pathology, Mayo Clinic and Mayo Foundation, Rochester, Minnesota . The Mayo Foundation is a part of the Graduate School of the University of Minnesota .
to ulceration within a diverticulum, and in a few instances such lesions have been seen . Actually, detailed pathologic studies of sufficient magnitude to allow determination of the frequency of such findings have not been published . McGrath [7], in rgr2, noted mucosal ulceration in eleven of twenty-seven surgical specimens, but he made no attempt to correlate this alteration with clinical findings. d e Quen'ain [2] described a "hemorrhagic form" of diverticulitis, about which he made this statement : "The patient is distressed, at times, by fairly severe intestinal hemorrhage, which clearly arises from ulcerative erosion of small vessels in the diverticulum ." It is impossible to determine whether or not de Quervain actually saw such ulceration, because pathologic studies were not included in his article . Synnott 112] stated that bleeding in diverticulitis originated in "eroding ulcerations of the mucosa lining the diverticulum or in small polyps in the diverticular area and not in the mucosa of the colon itself ." Again, corroborative pathologic studies were not presented . That ulceration within diverticula does account for some instances of bleeding was proved by Kocour [q], who reported a death caused by hemorrhage from an eroded artery in a diverticulum . Smith [it] reported the sigmoidoscopic visualization of several bleeding diverticula in a patient who had massive gastrointestinal hemorrhage . Young and Howorth [14] reported a case of diverticulitis and bleeding in which the surgical specimen contained numerous diverticula, several of which were inverted into the intestinal lumen . Ulceration was present on the mucosa of one of these inverted diverticula and this was considered to be the source of hemorrhage . These observers were unable to find any mention of inversion of diverticula in the literature . It appeared to them that an inverted diverticu-
the beginning of this century, diverticulitis of the colon has become a well recognized clinical and pathologic entity . More recently, its medical and surgical implications have been studied thoroughly and attempts have been made to establish the proper principles of management of this disease and its complications . Consequently, rather extensive information is available regarding the clinical and pathologic manifestations of acute diverticulitis, diverticulitis with perforation, diverticulitis with abscesses and diverticulitis with fistulas. Although hemorrhage in association with diverticulitis also has received considerable attention, information about this particular complication, especially regarding its pathogenesis, is not so nearly complete as might be desirable . Throughout the past fifty years, authorities on this subject repeatedly have warned physicians to search diligently for causes other than diverticulitis when rectal bleeding occurs . This is still sound advice despite the fact that bleeding can occur from diverticulitis alone . The frequency with which such bleeding occurs in cases of diverticulitis has been reported to be from 3 to 47 per cent, but the majority of studies report a frequency of ro to 30 per cent . The bleeding may be of any magnitude but is usually moderate in amount . The pathogenesis of bleeding directly attributable to diverticulitis has not been extensively investigated, although Neer [8], McGrath [7], Kocour [f], de Quervain [21, Young and Howorth [741, Lahey [6], Hoar and Bernhard [4], and Quinn and Ochsner [9] have made significant contributions . The bleeding usually has been attributed to ulceration of the colonic wall or INCE
American Journal
of
Surgery, V-1-me 94,
July, 1957
44
Bleeding in Colonic Diverticulitis Ium might bleed just as a polyp does when its surface becomes ulcerated . They pointed out that large vessels frequently are present about the bases of diverticula that might he the source of hemorrhage . Rosser [io] and Boyd [r] suggested that bleeding may arise from granulation tissue in diverticula that are the site of inflammation . Hickey 13] reported an unusual case in which an abscess had perforated into the inferior epigastric artery, with severe hemorrhage . Hoar and Bernhard [4] recently contributed valuable information regarding the pathologic findings in diverticulitis with bleeding . They found that forty-two of iii patients with diverticulitis had rectal bleeding . They examined pathologic specimens from three of these patients . In one specimen, four of five diverticula sectioned showed engorged granulation tissue replacing part of the mucosa . Ulceration was present in several of the diverticula in another specimen . The source of bleeding was not discovered in their third case . Of sixty-eight patients with divcrticulitis and diverticulosis reported by Noer [8], twenty had bleeding as a presenting or major symptom . Six of these patients underwent resection and specimens were examined pathologically in all six ; ulceration was found in one of the specimens . Bleeding from diverticulitis may occur in the presence of one of the other complications of the disease, or it may be the only complication present . The amount of blood lost is usually small or moderate, but in a significant number of cases it has been excessive, even to the point of being termed "exsanguinating ." Hoar and Bernhard [4] stated that most of the patients who have massive bleeding are more than sixty years of age and they frequently have arterial hypertension . It is often difficult to establish a clinical diagnosis of "bleeding diverticulitis ." Quinn and Ochsner [9] gave the following criteria that, when fulfilled, justify the assumption that the bleeding is from diverticulosis or diverticulitis : passage of gross blood per rectum ; evidence of diverticulitis or diverticulosis after use of a barium enema ; absence of other intrinsic lesions on rectal or proctoscopic examination ; roentgenographic studies demonstrating the stomach and small intestine to be normal . Thus, it is apparent that the diagnosis is often by exclusion .
The management of this complication of diverticulitis usually has been conservative, consisting of measures designed to put the intestine at rest, the administration of antibiotics and whole blood when indicated, and general supportive therapy . For the most part, this regimen has been adequate and surgical intervention has been used in the past only in those cases in which other indications for operation were present or in which the bleeding could not be controlled by medical means . Recently, however, surgical resection of the affected portion of colon has been used more extensively in the treatment of recurrent, persistent or severe hemorrhage . The present study was undertaken in an effort to correlate the pathologic features and the clinical manifestations of this complication of diverticulitis of the colon in the hope that such a correlation might contribute to better understanding and management of this disease . PRESENT STUDY
The diagnosis of diverticulitis of the colon was recorded for 1,970 patients at the Mayo Clinic from 1940 to 1954, inclusive . Of these patients, 145 (7 .4 per cent) gave histories of having passed blood by rectum for which no cause other than the diverticulitis could he found . Pathologic specimens preserved in formalin were available for examination in thirty-two of these 145 patients who had rectal bleeding . Thirty of these specimens were obtained during surgical resection of the affected colonic segments, whereas two specimens were obtained at necropsy . The clinical records of these thirty-two patients were examined for pertinent data relating to age, sex, symptoms, physical and laboratory findings, treatment, clinical course and follow-up studies . The findings at operation or necropsy were noted . The specimens were studied grossly with special reference to the appearance and thickness of the colonic mucosa, the presence or absence of ulceration, the diameter of the intestinal lumen, the thickness of the colonic wall, the presence or absence of zones of hemorrhage, the number of diverticula present, and the extent of diverticulitis . Multiple gross cross sections of the specimens were made for further examination of the areas of diverticulitis . Particular attention was paid to those regions in which extravasation of blood was 45
Mobley, Dockerty and Waugh evident. Blocks of tissue for microscopic study were taken from any obvious regions of ulceration or hemorrhage . Additional blocks of tissue were taken from any suspicious portions encountered during examination . Sections for microscopic examination were prepared and stained with hematoxylin and eosin in the usual manner . The original sections were available in ten of the thirty-two patients . All sections were studied to determine the characteristic picture present, and a search was made for any features that might account for the clinical bleeding . Six specimens of colon removed surgically for diverticulitis or one of its complications other than bleeding were picked at random for control specimens . These were examined in exactly the same manner as were the aforementioned thirty-two specimens .
one of the major complaints in fifteen patients . The most frequently noted physical findings and the number of cases in which each finding was encountered were abdominal tenderness (fifteen), extrarectal mass (nine), mass in the left lower abdominal quadrant (six) and intrarectal mass (two) . Although most of the patients had physical findings suggestive of diverticulitis, the results of examinations were completely negative in seven patients (22 per cent) . Results of routine laboratory studies were within normal limits except for the patient who had massive bleeding and in whom the value for hemoglobin was less than to gm . per loo ml . of blood . Proctoscopic examinations were performed on twenty-nine patients . Diverticula were seen in seven patients, and the findings were suggestive, but not diagnostic, of diverticulitis in nine others . Bleeding zones were seen in the intestinal mucosa in two patients . In one patient, an erroneous diagnosis of carcinoma was made . Entirely negative results of proctoscopic examination were recorded for seven patients . The three remaining patients had pathologic proctoscopic findings unrelated to the rectal bleeding . Roentgenologic examinations of the colon were done on thirty of the thirty-two patients . A definite diagnosis of diverticulitis was made in eighteen, and this diagnosis was suggested in four others . In the remaining eight patients, the radiologist considered a question of the presence of a neoplasm of the colon, but a definite roentgenologic diagnosis of carcinoma was reported in only one instance. Surgical exploration was performed on thirty-one of the thirty-two patients . Although rectal bleeding was frequently a major consideration in the decision to perform laparotomy, in only one patient was the problem of bleeding the sole surgical indication . The possibility of the presence of a malignant lesion undoubtedly influenced the decision to operate in many of these patients. Other indications were the existence of obstruction, the presence of an abdominal mass, and pronounced severity, persistence or recurrence of the symptoms of acute diverticulitis . Five different types of operative procedures were performed on the thirty-one patients just mentioned . Eleven underwent exteriorization procedures in which the affected loop of intes-
CLINICAL FINDINGS
Nineteen of the patients were men and thirteen were women . The range of age was from twenty-six to seventy-seven years, but only one patient was under forty . Five were in the fifth decade of life, thirteen were in the sixth decade and ten were in the seventh decade . Three patients were more than seventy years of age . Gross blood had been passed from the rectum by all the patients . The bleeding was often intermittent, and the blood usually was bright red . Bleeding was mild in twelve patients, moderately severe in nineteen and severe in one . Hemorrhage was the symptom that led the patient to seek medical care in seven instances (22 per cent) ; bleeding was the only symptom noted in six of these instances . The duration of bleeding varied considerably . Seventeen of the patients had noted blood in the stools for less than three months, whereas five patients had experienced bleeding for three months or more but less than a year . Ten patients had noted bleeding for a year or more, three of this latter group having observed it for more than five years. Rectal bleeding was overshadowed by other symptoms in twenty-five cases . In order of frequency, these were abdominal pain, chills, fever, diarrhea, decreased caliber of stools, constipation, dysuria and weakness . Although the presenting complaint was one other than bleeding, hemorrhage was recorded as being 46
Bleeding in Colonic Diverticulitis tine was brought out to the skin and subsequently excised, with extraperitoneal closure of the resulting colonic stoma as a final step . Primary resection with end-to-end anastomosis was performed in ten cases . Six patients underwent three-stage resection in which transversostomy preceded resection and anastomosis of the colon, the colonic stoma being closed later as a third stage. Three patients underwent primary resection and anastomosis with concomitant transversostomy and subsequent closure of the stoma . One patient underwent transversostomv but died before further surgical procedures could be performed. Except for this patient, all those treated surgically did well in the immediate postoperative period . Thrombophlebitis of the deep veins of one lower extremity developed in one patient but responded well to treatment . A fistula developed at the site of closure of the colonic stoma in another patient but later closed spontaneously . Twenty-four of the surviving patients have been followed up postoperatively for periods up to ten years . What was described as an episode of "intestinal obstruction" developed in one patient several years after operation ; he was hospitalized elsewhere and recovered with conservative management . The other twentythree patients have had no further symptoms attributable to diverticulitis . As previously indicated, two patients died . One died of peritonitis and bronchopneumonia after transversostomy . The other patient, who had massive rectal bleeding two weeks prior to admission, died of myocardial infarction . PATHOLOGIC FINDINGS
The length of colon that was resected varied from to to 35 cm ., the average being between Ig and zo cm . The zone of diverticulitis was in the sigmoid colon in twenty-seven patients and in the descending colon in four . Multiple regions of involvement were scattered from the ascending colon to the sigmoid in one patient . The pathologic findings generally were typical of those usually found in diverticulitis . Almost without exception there was segmental involvement characterized by pronounced edema. of the pericolonic tissues, thickening of the muscular wall, engorgement of blood vessels and, in more than half of the specimens,
narrowing of the intestinal lumen . For the most part, the inflammatory process appeared to involve small numbers of diverticula, even though multiple uninvolved diverticula might be present in other portions of the intestine . Microscopically, the intestinal wall and pericolonic tissues were infiltrated with polymorphonuclear leukocytes and, to a lesser extent, with mononuclear cells . The tissues were edematous and increased fibrous tissue could be found in the older lesions . The muscular layers of the intestine were thickened in many instances, particularly in those specimens in which the lumen was narrowed . In half of the specimens the mucosa was in polypoid folds which were so striking at times that they gave the appearance of true polyps . Flowever, close inspection revealed the true nature of the changes . Because of our particular interest in bleeding, a careful search for any changes pertaining to this was made . Gross examination revealed definite ulceration of the colonic mucosa in three specimens . Nineteen of the specimens had discolored zones in the mucosa suggestive of hemorrhage . Early in the gross study it was found that many areas of hemorrhage could be discovered by inspection of the colonic walls and the pericolonic regions . This proved to be one of the best methods of locating tissues from which bleeding might have originated . In eleven specimens, diverticula could he traced into, and grossly appeared to constitute aa part of, these hemorrhagic regions . An ulcerated inverted diverticulum was present in one specimen . Microscopic studies disclosed ulceration of the surface colonic mucosa in five other specimens in addition to the aforementioned three specimens in which ulceration was visible grossly. Microscopically, these ulcerated zones proved to be typical inflammatory ulcers characterized by absence of surface epithelium, destruction of the submucosa, vascular engorgement and evidence of acute inflammation . (Fig . I .) The ulceration in each of these eight instances was considered sufficient to produce bleeding, and good evidence of such bleeding was demonstrated in one section . Ulceration of the mucosa buried deeply in one or more diverticula was demonstrated microscopically in ten specimens . The microscopic picture of these ulcers was the same as that found in ulceration affecting the regular 47
Mobley, Dockerty and Waugh somewhere in the affected intestine, which is usually the sigmoid colon . This is borne out by the findings in the present study . In more than half of the specimens ulceration was noted in the colon or within diverticula . Other writers [4,8], have seen such ulceration in the intestines of patients who have bled from diverticulitis . It is assumed that such ulceration arises as a direct result of inflammation . It is possible that the trauma of the fecal current may contribute to the ulceration, but it appears that edema, exudation and necrosis of tissue could cause the ulceration within diverticula and that in the intestinal mucosa as well . It is not difficult to understand that bleeding may occur from a zone of diverticulitis that becomes ulcerated, especially in view of the pronounced vascular engorgement occurring within tissues affected by diverticulitis . One might wonder why bleeding does not occur more frequently . It is likely that many regions of ulceration were missed in the present study, because the method of gross serial sectioning employed was somewhat inadequate at best . Microscopic serial sectioning could be expected to increase the positive findings to a figure much nearer roo per cent than that reported herein . As already noted, one of our specimens contained an ulcerated inverted diverticulum . The possibility of this rare condition should be emphasized because of the danger of mistaking such a lesion for a polyp at proctoscopic examination . Cauterization or biopsy under such circumstances could produce serious consequences . The frequency with which diverticula could be traced into zones of gross hemorrhage and the microscopic demonstration of ulceration in these regions proved to be among the most interesting aspects of the present study . This occurred eleven times, and the microscopic findings were positive in eight cases. This would appear to be of significance, and it is possible that close attention to the involved segments of colon removed surgically in patients with clinical bleeding might reveal the source of bleeding in many instances . It might be well to re-emphasize the fact that a neoplasm of the colon is the cause of bleeding from the rectum far more frequently than is diverticulitis . Welch and associates [13] estimated that carcinoma of the colon is the cause of rectal bleeding five times as frequently as is diverticulitis . The presence of diverticu-
Frc . i . Colonic wall in diverticulitis with bleeding, demonstrating ulceration of the colonic mucosa. Note depth of penetration and the inflammatory reaction . Hematoxylin and eosin stain, original magnification
X 18 .
mucosa . Completely disrupted diverticula were seen in some sections, while less extensive ulceration was present in other specimens . (Figs . 2 and 3 .) In two instances in which microscopic ulceration of the colonic mucosa was found, additional ulceration within diverticula was present . In eight of the eleven specimens in which diverticula could be traced into regions of gross hemorrhage, microscopic examination revealed ulceration of the walls of the diverticula into the surrounding inflammatory hemorrhagic tissues . The extent of vascular engorgement in the inflamed tissues left little doubt that these ulcerated zones might be the source of significant bleeding . Thus, the gross and microscopic findings disclosed that eighteen (g6 per cent) of these thirty-two patients had ulceration either of the colonic wall or within diverticula . Similar studies of the control group of six specimens disclosed little difference in the over-all pathologic picture between the two groups of specimens . Absent in the control group, however, was evidence of hemorrhage or areas that might serve as sources of hemorrhage . Gross ulceration of the mucosa was absent, and microscopic examination failed to reveal any ulceration of the colonic wall or within diverticula . COMMENTS
It appears reasonable to assume that the origin of the bleeding in patients who have diverticulitis of the colon is from ulceration 48
Bleeding in Colonic Diverticulitis
Fir . 2. (a) and (h), Two examples of ulceration within a diverticulum in diverticulitis with bleeding . Hematoxylin and eosin stains, original magnification X i6 .
Fir . 3 . (a), Diverticulum with ulceration in diverticulitis with bleeding . Hematoxylin and cosin stain, original magnification X i6. (h), Wall of diverticulum shown in (a) . Note ulceration and surrounding inflammatory reaction . Hematoxylin and rosin stain, original magnification X 170.
49
Mobley, Dockerty and Waugh litis does not give any assurance that a concomitant carcinoma is not present . The aforementioned total of 1,970 patients surveyed in the present study included ion patients who had simultaneous diverticulitis and carcinoma . Carcinoma of the colon has received emphasis as the principal disease to be differentiated from diverticulitis in patients who have rectal bleeding, and it is probably the most important one. However, other diseases of the anal canal and colon must be considered in dealing with these patients . External and internal hemorrhoids, fissures, adenomatous polyps and ulcerative colitis are all capable of causing rectal bleeding . In addition, lesions of the upper part of the gastrointestinal tract, such as peptic ulcer, gastric neoplasm, Meckel's diverticulum and neoplasms of the small intestine, may produce bleeding that is difficult to differentiate from colonic bleeding. All these conditions must be considered before a diagnosis of diverticulitis with bleeding is made . The differentiation of these conditions frequently cannot be made until the time of operation, and occasionally the correct diagnosis cannot be made even then . The bleeding from diverticulitis characteristically is associated with other symptoms of diverticulitis, and a history of intermittent attacks may be obtained . However, 1q per cent of our thirty-two patients had bleeding as the only symptom . The bleeding usually is small or moderate in amount, but instances of massive bleeding have been recorded, as occurred in one of the patients in this study . The bleeding was often recurrent or intermittent in character . One-third of the patients gave histories of recurrent attacks of bleeding for more than one year . The bleeding often is a relatively minor symptom in the clinical picture, and the major complaints are those more characteristic of diverticulitis, such as abdominal pain, chills, fever, dysuria and diarrhea . Although the physical findings usually associated with diverticulitis may be present, the general examination may not be helpful insofar as the differential diagnosis of rectal bleeding is concerned, and sometimes the results of physical examination may be entirely normal . Proctoscopic and roentgenologic examinations have proved valuable in the study of these patients. About half of the patients who underwent proctoscopic examinations had find-
ings either diagnostic of or suggestive of diverticulitis . A definite roentgenologic diagnosis of diverticulitis was made in 6o per cent of the patients so examined . As useful as these examinations may be, it must be remembered that they are not infallible and that the presence of diverticulitis does not exclude the possibility of other disease . The management of patients who have "bleeding diverticulitis" usually has been conservative in the past . Such management appears reasonable for patients in whom the diagnosis can be definitely established and who exhibit bleeding for the first time . However, recurrent hemorrhage is not infrequent, and it is often impossible to exclude the possibility of malignant lesions. In these instances, it would be wiser to employ surgical therapy . Bleeding rarely is the only indication for surgical intervention in these patients ; only one patient in the present study had bleeding as the sole surgical indication . Some other complication of diverticulitis or doubt as to the nature of the pathologic process usually dictates the surgical approach . Generally speaking, indications for laparotomy in diverticulitis have been, and are, increasing. Indications for operation in "bleeding diverticulitis" probably will follow the same pattern. The surgical procedures performed for the patients in this study were predominantly multiple-stage resections, which have proved to be an adequate method of management, particularly for the extremely ill patient . Because of improved operative technics, better anesthesia, use of chemotherapeutic and antibiotic agents, and more efficient preoperative and postoperative care, primary resection of the colon recently has been used more frequently . The role of primary resection may increase in scope as surgical technics advance, but some patients still will require multiple-stage operations because of debility, extensive local disease or technical factors . The surgical procedure necessary in a given case is probably best decided in the operating room, where the extent of the disease can be evaluated . The final results of surgical therapy in the present group of patients have been satisfactory, although it is difficult to draw any extensive conclusions from such a small group. One patient died after transversostomy, death being due to perforation of the colon and peritonitis . The other patients who have been adequately 50
Bleeding in Colonic Diverticulitis followed up have (lone well except for minor complications .
REFERENCES BOYD, J . T934-
T. Diverticulosis and diverticulitis . Texas J . Med ., 43 : 681-685, 1948 . DE QUERVAIN, F . Dvverticulosis and diverticulitis of the large intestine . Practitioner, i IS : 352-360,
SUMMARY AND CONCLUSIONS
Detailed pathologic, clinical and follow-up studies have been made on thirty-one patients who underwent surgical treatment at the Mayo Clinic for colonic diverticulitis associated with bleeding and on one patient who died from myocardial infarction two weeks after massive rectal bleeding accompanying diverticulitis . Hemorrhage is a proved complication of diverticulitis . Although it is relatively rare, it must be considered in the differential diagnosis of rectal bleeding . The bleeding arises from ulceration of the affected colonic wall or ulceration within one or more diverticula . The bleeding is usually small or moderate in amount, is frequently recurrent over long periods and is usually associated with other symptoms of diverticulitis . It is difficult to differentiate bleeding due to diverticulitis from that due to neoplasm, and both diseases may occur simultaneously. The physical findings in "bleeding diverticulitis" are not characteristic . Roentgenologic and proctoscopic examinations are helpful in establishing a diagnosis, but neither should he considered infallible . In patients with diverticulitis, the complication of hemorrhage can be treated conservatively in many instances, provided that no doubt exists concerning the diagnosis . Surgical resection of the affected colon is justified in patients who have recurrent or uncontrollable hemorrhage, in those in whom the presence of a neoplasm cannot be excluded and in those who have indications for operation other than hemorrhage.
1927 . . HICKEY, R . 3-4-5
C . Massive colonic bleeding secondary to diverticulitis . Gastroenterology, 26 : 754-757, 1954 .
C. S . and BERNHARD, W . F . Colonic bleeding and diverticular disease of the colon . Surg., Gynec. e+Obst ., 99 : ioi - 107, 1954 . KocouR, E . J . Divcrticulosis of the colon : its incidence in 7,000 consecutive autopsies with reference to its complications. Am . J . Surg., 37 :
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433 -436, 1937
F . H. The advantages of an hepatic flexure Mikuliez type of defunctionalizing colostomy in the surgical treatment of diverticulitis . Label , Clin . Bull., 6 : 34 -37, 1 948 . MGGRATH, B . F . Intestinal diverticula : their etiology and pathogenesis ; with a review of twentyseven cases . Surg ., Gynec . er Obst., 15 : 429 444,
LAHEY,
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1912. 8 . NOER, R.
J . Hemorrhage as a complication of diverticulitis . Ann . Surg ., 141. 674-685 . 1955 9 . QUINN, W . C . and OcHSnnR, A . Bleeding as a complication of diverticulosis or diverticulitis of the colon. Am . Surgeon, 19 : 397 - 402, 195310 . RossER, C . Changing concepts concerning diverticulitis . J . Internat. Coll. Surgeons, 14 : 52-56, 1950 . II . SMITH, N . D .
Diverticulosis and diverticulitis : general consideration and sigmoidoscopic diagnosis . Am . J. Surg., 82 : 583-586, 1951 . cz. SY V VUTI', M . J . Diverticulitis . M . J. e- Rec ., 138 : 253 -257, 1933 . 13 . WELCH, C . F ., ALLEN, A . W . and DONALDSON, G . A . An appraisal of resection of the colon for diverticulitis of the sigmoid . Ann . Surg ., 138 : 332- 343-193314 . YOUNG, J . M . and HowoRTH, M . B ., JR. Massive
hemorrhage in diverticulosis : possible explanation of cause with presentation of case requiring surgical treatment . Ann . Sure ., 140 : 128-131,
51