Strictures of The Sigmoid: Barium Enema Evaluation: Colon

Strictures of the Sigmoid Colon: Barium Enema Evaluation -- Blakeborough et al. 220 (2)...
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(Radiology. 2001;220:343-348.) RSNA, 2001

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Strictures of the Sigmoid Colon: Barium Enema Evaluation1

Anthony Blakeborough, FRCR, Anthony H. Chapman, FRCP, FRCR, Sarah Swift, FRCR, Gary Culpan, MSc, Daniel Wilson, MSc and Maria B. Sheridan, FRCR
From the Departments of Radiology, St Jamess University Hospital, Beckett St, Leeds LS9 7TF, England (A.B., A.H.C., S.W., G.C., D.W., M.B.S.); and Royal Hallamshire Hospital, Sheffield, England (A.B.). From the 1997 RSNA scientific assembly. Received July 1, 1999; revision requested March 7, 2000; final revision received December 7; accepted January 4, 2001. Address correspondence to A.H.C. (e-mail: AnthonyHChapman@compuserve.com).
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ABSTRACT
PURPOSE: To assess the accuracy of radiologic interpretation, in the absence of clinical information, in the differentiation of benign and malignant sigmoid strictures at barium enema examination.
TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES
MATERIALS AND METHODS: On two occasions, four independent observers retrospectively assessed examination findings in 78 patients with documented sigmoid strictures (43 benign, 35 malignant). Each stricture was graded by using a fivepoint scale (definitely malignant to definitely benign).
RESULTS: No significant difference existed between the areas under the receiver operating characteristic curves for the two assessments with any observer. Consensus findings indicated agreement among at least three of the four observers in 68 (87%) and 66 (85%) cases at the first and second assessments, respectively. One benign stricture was called malignant at both assessments. When consensus existed, the positive predictive value for malignant strictures was 96% at both assessments (sensitivity, 63% and 66%).
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Strictures of the Sigmoid Colon: Barium Enema Evaluation -- Blakeborough et al. 220 (2)... Page 2 of 11
Nine malignant strictures were called benign, three at both assessments. When consensus existed, the positive predictive value for benign strictures was 84% and 88% at the first and second assessments, respectively (sensitivity, 88% and 86%, respectively). CONCLUSION: The differentiation between a benign and a malignant sigmoid stricture can be made in most cases at barium enema examination. When a stricture appears malignant, the diagnosis is usually correct, but caution is advised when a stricture appears benign. Index terms: Colon, stenosis or obstruction, 75.1281, 75.1282, 756.725, 756.726 Colon neoplasms, diagnosis, 75.1281, 75.1282, 756.31, 756.321, 756.33 Diagnostic radiology, observer performance Receiver operating characteristic (ROC) curve
INTRODUCTION
TOP ABSTRACT Sigmoid strictures are most frequently caused by carcinoma or INTRODUCTION diverticulitis. In 1940, Schatzki (1) stated, "The difficulty in MATERIALS AND METHODS differentiating diverticulitis, particularly of the sigmoid colon, from a RESULTS DISCUSSION carcinoma is as old as the knowledge of diverticulitis as a disease." REFERENCES Despite the multidisciplinary approaches of clinical examination, endoscopy, double-contrast barium enema examination, and computed tomography (CT), a gray area persists in the diagnosis of some sigmoid strictures, particularly when carcinoma and diverticular disease coexist or when a carcinoma causes perforation and a pericolic abscess develops (2). If a malignant stricture is called benign and managed conservatively, diagnosis will be delayed; even a 3-month delay can alter the stage of the disease, with a dramatic effect on therapeutic options and patient prognosis (3). If a benign stricture is called malignant, the opportunity for conservative management is lost.
A number of articles (46) have pointed out the advantages of using CT rather than barium enema examination when acute diverticulitis is clinically suspected. Diverticulitis can manifest indefinite clinical symptoms and signs (2); therefore, referral for barium enema examination is not unusual. When a sigmoid stricture is encountered at barium enema examination, radiologists need to know how certain a benign or malignant diagnosis can be. The purpose of our study was to address this need by determining the accuracy with which radiologists can differentiate between benign and malignant strictures when they interpret findings without clinical information.
MATERIALS AND METHODS

TOP
Cases from 78 double-contrast barium enema examinations were ABSTRACT INTRODUCTION selected from approximately 8,000 examinations performed at St MATERIALS AND METHODS Jamess University Hospital, Leeds, England, between 1991 and 1996. RESULTS DISCUSSION In the cases, the radiologic report made reference to a stricture in the REFERENCES sigmoid colon, and either definite histologic diagnosis or clinical and radiologic follow-up existed. None of the four observers (A.H.C., M.B.S., A.B., S.S.) played any role in case selection. There were 35 malignant and 43 benign strictures. Samples for histologic confirmation of all malignant
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lesions were obtained from surgical resection (n = 32), endoscopic biopsy (n = 1), or postmortem examination (n = 2). The diagnosis of benign stricture was established by means of surgical resection (n = 10) or clinical follow-up of at least 6 months, which included either endoscopic biopsy (n = 7) or flexible sigmoidoscopy and/or repeat double-contrast barium examination (n = 26). The malignant strictures (23 women, 12 men; age range, 4989 years; mean age, 74 years) included primary colonic carcinoma (n = 26); anastomotic recurrence of colonic carcinoma (n = 3); and metastases to the sigmoid colon from primary tumors of the pancreas (n = 2), stomach (n = 1), ovary (n = 1), breast (n = 1), or bladder (n = 1). The benign strictures (30 women, 13 men; age range, 2485 years; mean age, 65 years) consisted of both inflammatory and fibrotic strictures in association with diverticular disease (n = 34), inflammatory bowel disease (n = 3), radiation therapy (n = 1), ischemia (n = 1), inflammation from adjacent appendicitis (n = 1), or unknown conditions (n = 3). A standard double-contrast barium enema technique (7) had been used for all examinations. All patients had received a short-acting anticholinergic (Buscopan [hyoscine butyl bromide]; Boehringer Ingelheim, Germany; 20-mg intravenous administration) as an antispasmodic during the examination, and air had been used to insufflate the bowel. During each examination, a minimum of 10 views were acquired: right anterior and left posterior oblique views of the sigmoid, supine oblique view of the cecum, upright view of the hepatic and splenic flexures, vertical-beam posteroanterior view of the colorectum and angled prone view of the rectosigmoid, horizontal-beam cross-table view of the rectum, and right and left lateral decubitus views of the colorectum. Without any clinical information, the four independent observers and assessed the randomly sorted images from the 78 cases. All the images were made available to the observers. The observers recognized that an abrupt transition at the site of obstruction, destruction of mucosa, and apple-core configuration are considered malignant features, whereas a gradual zone of transition, preserved mucosal folds, and presence of diverticula are considered benign features (8). The observers were asked to grade the stricture by using one of the five following categories: 1, definitely malignant; 2, probably malignant; 3, indeterminate; 4, probably benign; and 5, definitely benign. The entire process was repeated after 3 months; again, no clinical information was provided, and cases were reviewed in random order. After the second assessment, the results of both assessments were analyzed. Receiver operating characteristic (ROC) methods (9) were used to construct ROC curves for each assessment by each observer, and the area under each curve was calculated. ROC curves demonstrated the trade-off between sensitivity for benign strictures and sensitivity for malignant strictures as the confidence threshold changed. Because the sensitivity for malignant strictures is the same as the specificity for benign strictures, the traditional ROC curve of sensitivity versus 1 - specificity for benign strictures was generated. The area under the ROC curve for each observer was calculated for each assessment, and the statistical significance of any differences between the first and second assessments for each observer was tested by using the method of Hanley and McNeil (10). The mean area under the ROC curve for the four observers was calculated for each assessment. The positive predictive value (PPV) for benign strictures was defined as the proportion of correct diagnoses of benign stricture of the total number of diagnoses of benign stricture. The PPV for malignant strictures
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was calculated as the proportion of correct diagnoses of malignant stricture of the total number of diagnoses of malignant stricture. This value was calculated by grouping grades 1 and 2 as diagnoses of malignant strictures and grades 4 and 5 as diagnoses of benign strictures. These predictive values represent the probability of each decision being correct. Sensitivity for malignant strictures was calculated as the number of correct diagnoses of malignant disease divided by the total number of malignant strictures. Sensitivity for benign strictures was calculated as the number of correct diagnoses of benign disease divided by the total number of benign strictures. Grades 1 and 2 were classified as diagnoses of malignant disease, and grades 4 and 5 were classified as diagnoses of benign disease. Consensus was defined when at least three of the four observers independently made the same interpretation. This consensus was used to identify those cases in which the majority of observers made the same decision and to highlight cases consistently misdiagnosed.
RESULTS
The ROC curves for each observer and the areas under the curves are shown in Figure 1. No significant difference existed between the two assessments for any observer (P > .05, Hanley and McNeil method [10]).
Figure 1. ROC curves are similar for all four observers (interobserver variation) and for the first and second assessments (intraobserver variation). Areas under the curves at assessments 1 and 2, respectively, were as follows: observer 1 (1), 0.87 and 0.94; observer 2 (2), 0.89 and 0.90; observer 3 (3), 0.88 and 0.92; observer 4 (4), 0.91 and 0.89; and mean, 0.89 and 0.91.
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The Table shows the results of observer classification of strictures. The mean numbers of decisions made at the first and second assessments were 73 (PPVs: benign strictures, 82%; malignant strictures, 94%) and 71 (PPVs: benign strictures, 86%; malignant strictures, 92%), respectively. The mean percentage of indeterminate (grade 3) decisions was 8% (six of 78 decisions; first assessment, five of 78; second assessment, seven of 78). The mean number of correct decisions for both assessments was 63, resulting in an accuracy of classification of 81%. At both assessments, consensus was reached in a similar proportion of cases. At the first assessment, consensus was reached in 68 of 78 cases, of which 60 (77%) were correctly identified as benign or malignant. At the second assessment, consensus was reached in 66 cases, of which 60 (77%)
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were correctly identified as benign or malignant. The numbers of diagnoses of malignancy for each observer are presented in the Table. The sensitivity range for the diagnosis of malignant strictures was 60%74% (PPV, 93%96%) for the first assessment and 63%80% (PPV, 90%96%) for the second. With consensus, the sensitivities for the diagnosis of malignant strictures were 63% (PPV, 96%) and 66% (PPV, 96%) at the first and second assessments, respectively. With the incorrect diagnoses of malignancy, the same benign stricture was called malignant by three of four observers (consensus) at both assessments. This case involved a 24-year-old patient with known small-bowel Crohn disease that extrinsically involved the sigmoid colon and produced an eccentric shouldered stricture (Fig 2). In three other benign cases, the observers did not reach consensus at either assessment; these cases all involved diverticular strictures.
Figure 2. Horizontal-beam cross-table double-contrast barium enema radiograph of the rectum shows an inflammatory distal sigmoid stricture (between arrows) due to extrinsic involvement from adjacent smallbowel Crohn disease. The rectum is at the top of the image. The margin appears shouldered (arrowheads), which resulted in a diagnosis of malignancy. Diagnosis was made by consensus at both assessments in the absence of clinical information.
The sensitivity range for the diagnosis of benign strictures was 88%95% (PPV, 77%87%) for the first assessment and 88%91% (PPV, 83%93%) for the second (Table). At consensus, the sensitivities for the diagnosis of benign strictures were 88% (PPV, 84%) and 86% (PPV, 88%) for the first and second assessments, respectively. With the incorrect benign decisions, three malignant strictures were called benign by at least three of four observers (consensus) at both assessments. These cases all involved primary sigmoid carcinomas. Two were associated with local perforation, and the other was a tumor showing submucosal infiltration (Figs 3, 4). Six other malignant strictures were also considered benign by consensus at one of the two assessments. Two strictures were primary sigmoid cancers: One was a small tumor in a segment of diverticular disease (Fig 5), and the other was a large tumor with extensive local invasion (Fig 6). The other four were extracolonic primary malignancies from the bladder, breast, ovary, and pancreas involving the sigmoid colon (Fig 7). One malignant case in which the observers did not reach consensus at either assessment involved an anastomotic recurrence of a primary sigmoid carcinoma.
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Figure 3. Right anterior oblique double-contrast barium enema radiograph of the sigmoid shows perforated sigmoid carcinoma with pericolic abscess formation. Diverticula (arrowheads) are present proximal and distal to the stricture, the distal margin is tapered (long arrows), and subserosal tracking is present at the proximal end of the stricture (short arrows). All observers reported this as benign at both assessments. View larger version (119K): [in this window] [in a new window] [Download PPT slide]
Figure 4. Right anterior oblique double-contrast barium enema radiograph of sigmoid shows sigmoid carcinoma with submucosal infiltration. Margins of the stricture are tapered (arrows), and intact mucosal folds run through the stricture (arrowheads). All observers reported this as benign at both assessments.
Figure 5. Right anterior oblique double-contrast barium enema radiograph of the sigmoid shows diverticulitis with localized sigmoid perforation and coexisting Dukes C carcinoma. The stricture has tapered proximal margins (long solid arrows), although slight shouldering at the distal margin (open arrows) is present. Barium is leaking ( ) into a pericolic collection that contains gas (arrowheads), and a tract at the proximal end (short solid arrows) connects with the bowel lumen. This was called benign by consensus at both assessments. View larger version (143K): [in this window] [in a new window] [Download PPT slide]
Figure 6. Right anterior oblique double-contrast barium enema radiograph of sigmoid shows the sigmoid carcinoma with
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submucosal and extensive local invasion and shows a long stricture with tapered margins (arrows). Intact mucosal folds (arrowheads) can be seen at the proximal end of the stricture. This was called benign by consensus at the first assessment.
Figure 7a. Right anterior oblique double-contrast barium enema radiograph of the sigmoid. (a) Sigmoid involvement from peritoneal deposits of ovarian carcinoma. A diverticulum (white arrowhead) is seen at the proximal end of the stricture and is one of many scattered around the colon. Stricture shows tapered margins (large arrows) and intact mucosal folds (black arrowheads). Projections (small arrows) from the lumen were misinterpreted as necks of diverticula. Clinical information was withheld from the observers, who all reported the stricture as benign at the first assessment. (b) Sigmoid involvement from peritoneal deposits of pancreatic carcinoma. Stricture with intact mucosal folds (arrowheads) and tapered margins (arrows) is depicted. Diverticula were present elsewhere in the colon. Clinical information was withheld from the observers, who all reported the stricture as benign at the first assessment.
Figure 7b. Right anterior oblique double-contrast barium enema radiograph of the sigmoid. (a) Sigmoid involvement from peritoneal deposits of ovarian carcinoma. A diverticulum (white arrowhead) is seen at the proximal end of the stricture and is one of many scattered around the colon. Stricture shows tapered margins (large arrows) and intact mucosal folds (black arrowheads). Projections (small arrows) from the lumen were misinterpreted as necks of diverticula. Clinical information was withheld from the observers, who all reported the stricture as benign at the first assessment. (b) Sigmoid involvement from peritoneal deposits of pancreatic carcinoma. Stricture with intact mucosal folds (arrowheads) and tapered margins (arrows) is depicted. Diverticula were present elsewhere in the colon. Clinical information was withheld from the observers, who all reported the stricture as benign at the first assessment.
DISCUSSION
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Double-contrast barium enema examination is frequently used to TOP ABSTRACT investigate suspected lower gastrointestinal tract disease, because it can INTRODUCTION be used to evaluate the bowel mucosa and lumen and to identify sinus MATERIALS AND METHODS RESULTS tracts and fistulas. Despite widely accepted features that characterize DISCUSSION benign inflammatory and malignant lesions, difficulties in the REFERENCES differentiation of some diverticular and neoplastic strictures of the sigmoid colon persist (11). Recent advances in both imaging and direct endoscopic examination of the lower gastrointestinal tract have showed promise in solving this problem. Unfortunately, endoscopy is not the sole solution. Although malignancy can often be diagnosed with confidence at biopsy, negotiation of a sigmoid colon with diverticular disease may be difficult because of an increased risk of perforation, or it may fail (12). When acute diverticulitis is suspected clinically, CT may be preferred to barium enema examination because it can be used to define the extent of disease and to depict pericolic inflammatory changes and abscess formation (1317). It can be used to examine the abdomen and pelvis for distant signs of malignant disease and to diagnose other pathologic conditions in the absence of sigmoid diverticulitis (4). CT findings such as bowel wall thickening and diverticulosis are nonspecific. Fluid at the root of the mesentery and vascular engorgement are signs of mesenteric inflammation that suggest diverticulitis (18), whereas the presence of pericolic lymph nodes and luminal masses are more frequent in patients with colonic carcinoma (19,20). Balthazar et al (17) estimated that in approximately 10% of patients CT could not be used to confidently diagnose acute diverticulitis. However, in a larger blinded study (20), CT had relatively low accuracy in the differentiation of diverticulitis and carcinoma; unequivocal diagnosis was possible in only 49% of cases. Clinical details are of value (21). Medical historysuch as one of inflammatory bowel disease, previous colonic resection, or previous non-colonic malignancyalter bias and decision making when radiologic studies are interpreted. However, in practice, a diagnosis is often made even when the clinical details are unhelpful or nonspecific. Therefore, the purpose of this study was to evaluate the accuracy of radiologic interpretation in the absence of clinical information. The use of multiple observers allowed assessment of inter- and intraobserver variability, and, by looking for consensus between the observers, difficult cases that were consistently misinterpreted were highlighted. The ROC values obtained indicate a high degree of accuracy for all observers. When consensus in the diagnosis of a malignant stricture occurred, the diagnosis was correct in all cases but one: that of the patient with a Crohn stricture. All strictures called malignant at consensus, except one Crohn stricture, were correct. This finding suggests that a high degree of confidence can be attached to a radiologic interpretation of a malignant stricture. In the erroneous case, if the clinical details had been known, the interpretation would likely have been different. In clinical practice, these details would almost certainly have been known. The cases causing worry were the malignant lesions (four extracolonic malignancies, five carcinomas) that were called benign by consensus at one or both assessments and the anastomotic recurrence for which a consensus was not reached. Anastomotic recurrence or extrinsic malignant infiltration from an extracolonic malignancy may simulate a benign stricture, because in such cases the mucosa may remain intact, and the margins of the stricture may be tapered. Coexisting diverticula may lead the radiologist to think of an
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inflammatory stricture, although diverticula may coexist with malignant strictures; they have been shown to be present in 28% of sigmoid carcinomas (22). Extrinsic malignant infiltration is recognized at barium enema examination as crenulation of the margin of the bowel and plicated folds seen en face. Such changes are not always apparent, and pericolic inflammation can produce a similar appearance. Nevertheless, in patients with a history of extracolonic malignancy or resected colonic cancer, recurrent disease is the diagnosis foremost in the mind of the clinician and radiologist, regardless of the appearance at doublecontrast barium enema examination. Should a diagnosis of a benign stricture still be entertained, further investigation with CT, magnetic resonance imaging, endoscopy, or even surgery would be performed almost as a matter of course. Of greater concern are the primary sigmoid malignancies, with or without diverticulosis and its complications, which had sufficiently atypical appearances that our observers called them benign. Submucosal infiltration and carcinomas that had perforated with associated inflammation resulted in misdiagnosis by most of the observers. Submucosal infiltrating tumors may have features that are usually considered benign; the stricture may be long and have intact mucosa and tapered margins. Inflammation associated with a carcinoma that has perforated may mask the underlying tumor and result in a stricture that resembles diverticulitis. The radiologic features that we use to differentiate benign and malignant lesions are relatively nonspecific and not infallible. Continued caution must be exercised when sigmoid strictures are called benign at barium enema examination, and we should be reassured that the suggestion of an alternative test, such as endoscopy, CT, or early-interval repeat double-contrast barium enema examination, is the correct course of action.
FOOTNOTES
Abbreviations: PPV = positive predictive value, ROC = receiver operating characteristic Author contributions: Guarantor of integrity of entire study, A.H.C.; study concepts, A.H.C., A.B.; study design, A.B.; literature research, S.S.; clinical studies, A.H.C., M.B.S., A.B., S.S.; data acquisition, A.H.C., M.B.S., A.B., S.S.; data analysis, G.C.; statistical analysis, D.W.; manuscript preparation, A.H.C., A.B., S.S.; definition of intellectual content, A.H.C., A.B.; manuscript editing and review, A.H.C.; manuscript final version approval, A.B., A.C.H., D.W.
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5. Cho KC, Morehouse HT, Alterman DD, Thornhill BA. Sigmoid diverticulitis: diagnostic role of CTcomparison with barium enema studies. Radiology 1990; 176:111-115.[Abstract] 6. Hulnick DH, Megibow AJ, Balthazar EJ, Naidich DP, Bosniak MA. Computed tomography in the evaluation of diverticulitis. Radiology 1984; 152:491-495.[Abstract] 7. Laufer I. Double contrast gastrointestinal radiology with endoscopic correlation Philadelphia, Pa: Saunders, 1979; 497-498. 8. Balthazar EJ. Diverticular disease. In: Gore RM, Levine MS, eds. Textbook of gastrointestinal radiology. 2nd ed. Philadelphia, Pa: Saunders, 2000; 924. 9. Metz CE. ROC methodology in radiological imaging. Invest Radiol 1986; 21:720-733.[Medline] 10. Hanley JA, McNeil BJ. A method of comparing the areas under receiver operating characteristic curves derived from the same cases. Radiology 1983; 148:139-143. 11. Rowe RJ, Kollimar GH. Collective review: diverticulitis of the colon complicated by carcinoma. Surg Gynecol Obstet 1952; 94:1-9. 12. Aste H, Pugliese V, Munizzi F, Giacchero A. Left-sided stenosing lesions in colonoscopy. Gastrointest Endosc 1983; 29:18-20.[Medline] 13. Johnson CD, Baker ME, Rice RP, Silverman P, Thompson WM. Diagnosis of acute colonic diverticulitis: comparison of barium enema and CT. AJR Am J Roentgenol 1987; 148:541-546. [Abstract/Free Full Text] 14. Balthazar EJ, Megibow AC, Hulnick D, Naidich DP. Carcinoma of the colon: detection and preoperative staging by CT. AJR Am J Roentgenol 1988; 150:301-306.[Abstract/Free Full Text] 15. Neff CC, vanSonnenberg E. CT of diverticulitis: diagnosis and treatment. Radiol Clin North Am 1989; 27:743-752.[Medline] 16. Mueller PR, Saini S, Wittenberg J, et al. Sigmoid diverticular abscesses: percutaneous drainage as an adjunct to surgical resection in 24 cases. Radiology 1987; 164:321-325.[Abstract] 17. Balthazar EJ, Megibow A, Schinella RA, Gordon R. Limitations in the CT diagnosis of acute diverticulitis: comparison of CT, contrast enema, and pathologic findings in 16 patients. AJR Am J Roentgenol 1990; 154:281-285.[Abstract/Free Full Text] 18. Padidar AM, Jeffrey R, Mindelzun RE, Dolph JF. Differentiating sigmoid diverticulitis from carcinoma on CT scans: mesenteric inflammation suggests diverticulitis. AJR Am J Roentgenol 1994; 163:81-83.[Abstract/Free Full Text] 19. Chintapalli KN, Esola CC, Chopra S, Ghiatas AA, Dodd GD 3rd. Pericolic mesenteric lymph nodes: an aid in distinguishing diverticulitis from cancer of the colon. AJR Am J Roentgenol 1997; 169:1253-1255.[Abstract/Free Full Text] 20. Chintapalli KN, Chopra S, Ghiatas AA, Esola CC, Fields SF, Dodd GD, III. Diverticulitis versus colonic cancer: differentiation with helical CT findings. Radiology 1999; 210:429-435. [Abstract/Free Full Text] 21. Simpkins KS, Young AC. The differential diagnosis of large bowel strictures. Clin Radiol 1971; 22:449-457.[CrossRef][Medline] 22. Ponka LL, Fox JD, Brush C. Coexisting carcinoma and diverticula of the colon. Arch Surg 1959; 79:373-384.
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(Radiology. 2001;220:343-348.) RSNA, 2001

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MATERIALS AND METHODS

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