There are limited data about follow-up colonoscopy after a CT diagnosis of acute diverticulitis, and the pooled prevalence of colorectal cancer in a small number of patients is only slightly higher than the calculated prevalence of colorectal cancer in a population of comparable age.
Abstract
Purpose:
To estimate the prevalence of underlying adenocarcinoma of the colon in patients in whom acute diverticulitis was diagnosed at computed tomography (CT) and to compare that to the prevalence of colon cancer in the general population.
Materials and Methods:
A comprehensive literature review was performed to find articles in which patients with CT diagnosis of acute diverticulitis underwent surgery, colonoscopy, or barium enema study within 24 weeks. Patients meeting these criteria were included for analysis. A pooled prevalence of cancer was calculated on the basis of a random effects model and compared qualitatively with the prevalence of cancer in the general population. The 95% confidence intervals around the prevalence of cancer in the study populations were determined.
Results:
Ten articles met the inclusion criteria. Data from these articles included only 771 patients who underwent surgery, colonoscopy, or barium enema study within 24 weeks of diagnosis. Fourteen patients were found to have colon cancer, for a prevalence of 2.1% (95% confidence interval: 1.2%, 3.2%). This compares to a calculated estimated prevalence of 0.68% among U.S. adults older than 55 years.
Conclusion:
There are limited data to support the recommendation to perform colonoscopy after a diagnosis of acute diverticulitis.
© RSNA, 2012
Introduction
Acute diverticulitis results from inflammation of a colonic diverticulum. It usually has an uncomplicated course, manifesting primarily as pain; however, some patients may have abscesses, fistulas, obstruction, and/or perforation at presentation. Acute diverticulitis imposes an important clinical burden on health care systems, resulting in more than 300 000 hospital admissions and $2.5 billion in cost annually (1,2). Computed tomography (CT) of the abdomen is often the diagnostic test of choice, with sensitivity, specificity, and positive and negative predictive values all well greater than 95%. Because CT features of acute diverticulitis (eg, thickening of the bowel wall) can also be present in carcinoma of the colon (3–7), professional societies such as the American Society of Colon and Rectal Surgeons and the American College of Gastroenterology recommend that patients undergo colonoscopy to exclude colon cancer after an episode of acute diverticulitis (8,9). The data supporting this recommendation, however, are sparse and largely based on small cohorts and/or case reports. Given the number of admissions for diverticulitis, an understanding of the impact of such a practice is important.
To our knowledge, no systematic evaluation has been performed to determine what proportion of patients who undergo colonoscopy after a presumed episode of acute diverticulitis actually have an underlying carcinoma of the colon. To this end, the purpose of this study was to estimate the prevalence of underlying adenocarcinoma of the colon in patients in whom acute diverticulitis was diagnosed at CT and to compare that to the prevalence of colon cancer in the general population.
Materials and Methods
Literature Review Protocol
The databases used included PubMed, EMBASE, BIREME, and the Cochrane Library. A librarian assisted with the electronic search. The following search terms were used: colon cancer, colonoscopy, and diverticulitis, including qualifiers that permitted the inclusion of words regardless of their suffix. No predetermined study design type, language limits, or publication year was included to limit the search. The literature review started on December 18, 2010, and the date of the last search was June 13, 2011.
Study Eligibility and Selection
Eligibility criteria were established before the literature search. Studies were eligible for inclusion if patients received a diagnosis of acute diverticulitis at CT and subsequently underwent colonoscopy, surgery, or barium enema study within 24 weeks of CT. Two researchers (V.F.S., a 3rd-year diagnostic radiology resident, and A.C.W., an abdominal fellowship–trained radiologist with 7 years of experience) screened the initial search results on the basis of article title and abstract. The full articles of relevant studies were retrieved and additional searches of their bibliographies performed to identify additional relevant studies not identified in the initial search. The reviewers then applied the inclusion criteria to all potentially relevant studies. Data from studies that met the inclusion criteria were extracted and tabulated. If there was suggestion of overlap of the cohorts among the included studies, only data from the most comprehensive cohort were included.
Data Extraction and Summary Measures
Two reviewers (V.F.S. and A.C.W.) performed data extraction in consensus. From each study the following were abstracted: (a) authors, (b) type of publication, (c) country where the study was performed, (d) year of publication, (e) average age of patients, (f) total number of eligible patients, (g) number of colon cancers diagnosed, (h) location of the colon cancers, if available, (i) type of follow-up, and (j) any additional information regarding the nature of the cohort.
Data and Statistical Analysis
The primary outcome of the systematic review was the percentage of patients with colon cancer who had an initial diagnosis of diverticulitis at CT. For each study, we calculated the exact 95% confidence intervals around the prevalence of cancer in the study population. We calculated the pooled estimate and 95% confidence intervals based on a random effects model by using the meta-analysis routine of Stata 11.2 (StataCorp, College Station, Tex). Arcsine transformation was applied to the prevalence estimates to stabilize variances and meet the assumption of normality (10). These were later back-transformed to actual prevalences.
A forest plot was used to graphically depict the amount of heterogeneity among studies (11). A x2 heterogeneity test examined the null hypothesis that the true prevalences are identical in every study (12,13). In addition, an I2 statistic was used to measure the variation in the effect size attributable to heterogeneity rather than sampling error (12,13).
Publication bias was assessed visually and formally by using Stata’s metabias funnel plot asymmetry test (14,15). The prevalence of colon cancer in the population was calculated by using data from the 2008 U.S. Census, with the number of patients older than 55 years as the denominator and the 5-year limited duration prevalence of colon cancer obtained from the U.S. National Cancer Institute’s Surveillance Epidemiology and End Results database as of January 1, 2008, as the numerator (16). The arbitrary selection of 55 years as the age cutoff is based on the lower limit of the age range of patients with acute diverticulitis in the analyzed studies.
A limited-duration prevalence represents the proportion of people alive on a certain day who received a diagnosis of the disease within a specified number of years in the past. We opted to use the limited-duration prevalence because it is a relevant number for the context (as it excludes people who are deceased, as opposed to the complete prevalence) and because it is a conservative measurement, as any bias would be in the direction of showing a greater difference between the prevalence of colon cancer in the general population and in our study population. The use of the 5-year time frame for the limited-duration prevalence is based on the fact that patients are generally not considered cured until 5-year follow-up has been completed (17).
Results
Study Selection
The flowchart for the systematic review is shown in Figure 1. A total of 490 unique publications were initially identified in the literature search, from which 15 were included on the basis of title and abstract. Review of the bibliographies of these articles generated eight additional relevant articles. The full texts of these 23 articles were retrieved and reviewed, and the application of inclusion criteria resulted in a total of three abstracts and nine relevant articles, two of which (Ambrosetti et al [18,19], published in 1997 and 2002) were excluded given the high likelihood of duplicate cohorts. The exclusion was based on substantial overlap in time frames of patient recruitment by the same investigators in the same institution as well as identical descriptions of patients with false-positive diagnoses of diverticulitis. Only the most comprehensive publication by that group of authors (Ambrosetti et al [20], published in 2000) was included in the analysis. There was complete agreement among the authors as to the inclusion of the studies.
Figure 1:
Flowchart of systematic literature review.
Patient Cohort
Of the 10 studies included in this systematic review, six were performed in the United States. One study each was performed in France, Switzerland, Israel, and Australia. A total of 771 patients had a CT diagnosis of diverticulitis and underwent a follow-up examination within 24 weeks of CT. The number of patients enrolled per study ranged from 11 to 224. Follow-up was performed with surgery in 253 patients, colonoscopy in 430, and surgery, colonoscopy, or barium enema study in 88 (7,21). Fourteen patients were found to have colon cancer, which was diagnosed with surgery in three patients, colonoscopy in nine, and surgery, colonoscopy, or barium enema study in two. Only Pradel et al (21) described the locations of the diverticulitis. These results are summarized in the Table.
Study and Patient Characteristics
Numbers in parentheses are ranges. NA = not available.
Data are numbers of patients included in analysis.
Article is an abstract.
Statistical Analysis
As shown in Figure 2, the estimated pooled prevalence of colon cancer detected at follow-up after the CT diagnosis of diverticulitis was 2.1% (95% confidence interval: 1.2%, 3.2%). Results of the funnel plot asymmetry test for publication bias were not significant (P = .88), suggesting no major publication bias (Fig 3). There was no evidence of heterogeneity among studies (I2 = 0%, P = .861).
Figure 2:
Forest plot of the included studies and the prevalence of colon cancers detected. CI = confidence interval.
Figure 3:
Results of the funnel plot asymmetry test for publication bias, along with pseudo 95% confidence limits for the summary estimate, suggest no major publication bias. 5% = pseudo 95% confidence limits.
Colon Cancer Prevalence in the General Population
On the basis of data from the U.S. National Cancer Institute’s Surveillance Epidemiology and End Results program, 478 669 people had active colon cancer based on the 5-year limited duration prevalence as of January 1, 2008 (16). U.S. Census data from the same year puts the population older than 55 years at 70 092 000 (27). With use of these figures, the prevalence of active colon cancer in patients older than 55 years was calculated to be 0.68%.
Discussion
Results from this systematic literature review show that there are very limited data about follow-up colonoscopy after CT diagnosis of acute diverticulitis. Although the prevalence of colon cancer calculated in the small number of patients who had undergone follow-up was higher than that in the general population (2.1% vs 0.68%, respectively), the data from which this percentage was derived were mostly extracted from studies not designed to answer our question. The only study designed to answer this question was performed by Lahat et al (25), who found that three of 224 patients (1.3%) had colon cancer at follow-up. It is likely that the prevalence of colon cancer in patients suspected of having diverticulitis is lower than 2.1% owing to selection bias, with many excluded patients undergoing clinical follow-up rather than surgery, colonoscopy, or barium enema study because these patients may be perceived as having a lower risk of cancer. This is particularly evident in the study by Ambrosetti et al (20), in which only 136 of 420 patients underwent surgery and thus met the inclusion criteria for the study; the remaining 284 patients were excluded because they only underwent clinical follow-up.
Our calculated prevalence is likely further overestimated due to the characteristics of the subjects in studies advocating follow-up. Two of the studies included in our data set described many patients who were found to have suspicious lesions at CT, which likely exaggerated the true prevalence of colon cancers. These include the study by Ryan et al (7), who found a mass at CT in 20 of 117 patients—three of whom received a diagnosis of colon cancer at surgery. Another study, by Elramah et al (6), found a masslike lesion in seven of 115 patients, from which two cancers were later found. Clearly, if a masslike lesion is found in the setting of acute diverticulitis, appropriate follow-up to exclude an underlying cancer is warranted. However, current guidelines do not discriminate on which findings or clinical presentations associated with acute diverticulitis at CT are concerning enough to recommend follow-up colonoscopy routinely. In addition, some studies were published before the advent of multidetector CT, when the diagnosis of diverticulitis was made by means of barium enema study or single-detector CT (4,7,20).
Assuming that our calculated 2.1% prevalence of colon cancer in patients with a CT diagnosis of diverticulitis indeed reflects the true prevalence, it more closely approximates the prevalence of colon cancer in the asymptomatic general population than in the symptomatic population; for example, patients undergoing colonoscopy because of positive fecal occult blood test results have a much higher rate of colon cancer, ranging from 6.4% to 9.4% in separate studies (28–30). The yield of colonoscopy is thus much higher when performed for this laboratory finding, which in itself is relatively nonspecific. Despite the apparent threefold increase in the prevalence of colon cancer in patients with a CT diagnosis of diverticulitis, we believe that the higher specificity of CT for colon cancer does not justify the broad recommendation of follow-up colonoscopy to exclude cancer and that more refined criteria should be developed.
In fact, the practice of performing colonoscopy after presumed diverticulitis to exclude colon cancer appears to have in large part arisen from concern of colon cancer simulating the appearance of diverticulitis at CT (3,31). The isolated finding of colonic wall thickening appears to be associated with colon cancer, which may be a mimicker of diverticulitis (32–36). Although colonic wall thickening by itself is nonspecific, many authors have validated findings that accurately point to a diagnosis of diverticulitis, including inflamed diverticula, pericolic fat stranding, fluid at the mesentery, and a preserved bowel enhancement pattern (37–40). With use of these criteria, the overall accuracy of CT for the diagnosis of acute diverticulitis has been shown to be approximately 99% (22,39). Thus, the definitions of what constitutes diverticulitis versus colon cancer at CT may have affected the prevalence of colon cancer in published studies. Because some of the colon cancers concurrent with “diverticulitis” in fact represented inaccurate diagnoses of diverticulitis (31,41,42), the likelihood of underlying colon cancer in patients with diverticulitis will be lower when the diagnosis of diverticulitis is unambiguous. More recently, some authors have demonstrated the potential of CT perfusion as a tool to help resolve this occasional ambiguity, which may serve to further reduce the number of inaccurate CT diagnoses (43).
Although the performance of colonoscopy is recommended in some guidelines (8,9), several authors have disputed the notion that follow-up colonoscopy is necessary after an episode of acute diverticulitis (with the exception of age-appropriate colonoscopic screening). In a prospective study aimed at understanding the risks and benefits of early versus late colonoscopic follow-up in diverticulitis, Lahat et al (42) suggested that colonoscopy performed immediately after an episode of acute diverticulitis adds no clinical value. In a retrospective study, Lam et al (44) showed that the prevalence of colon cancer in patients with diverticulitis is lower than the lifetime risk of colon cancer. In a case-control study, Chintapalli et al (40) believed that the specificity of CT findings of diverticulitis and colon cancer is so high that an unequivocal diagnosis can be made with 100% accuracy for both diseases. In a smaller cohort, Lau et al (26) found no cases of colon cancer at colonoscopic follow-up of diverticulitis and believed that colonoscopic evaluation after diagnosis of diverticulitis is unjustified. Finally, Anglade et al (45) found no statistically significant difference in findings at colonoscopy in patients after an episode of acute diverticulitis compared with a control screening population. Clearly, some percentage of patients who have diverticulitis will also have a concurrent colorectal cancer. Our synthesis of the current literature suggests only a trend toward a higher percentage than that expected in the background population.
Despite the association of both diverticulitis and colon cancer in patients with diets high in animal fat and low in fiber (46–48), epidemiologic studies have not definitively established a clear relationship between diverticulosis and colon cancer (46–50). Some have further suggested that the two diseases many arise separately (51). If diverticulitis itself irrespective of imaging findings does not portend a higher risk for colon cancer, the addition of colonoscopy may only serve to reduce the diagnostic uncertainty at CT, which the literature suggests is minimal. Although the benefits of age-appropriate screening colonoscopy cannot be overemphasized, the risks and costs of performing the procedure in all patients presumed to have diverticulitis are often overlooked. Results from large cohorts describe the rate of serious complications from colonoscopy (eg, perforation, myocardial infarction, or stroke) to be around 0.1%–0.2% (52,53), which could generate significant morbidity if performed on each of the estimated 120 000 cases of diverticulitis annually (54). With an estimated Medicare reimbursement of $300, which does not include facility fees, the calculated annual cost of at least $36 million is considerable (55,56).
The limitations of this study include verification bias and lack of a control population. The relatively low number of patients meeting the inclusion criteria also limits a rigorous assessment of its merits. The lack of a control group necessitates comparison with data from the general population such as those found in population-based registries. We opted for using data from the U.S census, which has been used in other research projects (57–59) and is considered the official population number. In addition, we chose to use the Surveillance Epidemiology and End Results database to estimate the colon cancer prevalence because it is one of the most reliable cancer registries in the United States and because of the wide variability in reported frequencies of colon cancer in the asymptomatic general population, which ranges from 0.16% to 1.2% (60–64). Our estimated prevalence of 0.68% is an intermediate number within the range of these published data and is therefore a valid and representative number of the population in our study. Regardless of the true prevalence within this range, we believe that a more refined approach to recommending colonoscopy after a CT diagnosis of acute diverticulitis should be considered. A definitive study would require a large cohort of patients willing to undergo colonoscopy after an episode of acute diverticulitis. Such a study would be difficult and limited by self-selection bias because patients with persistent symptoms are more inclined to undergo colonoscopy after acute symptoms have resolved (42). Finally, some of the data included in the study were obtained from abstracts that have not been published. We believed this was an appropriate option to maximize the available data and minimize publication bias.
In conclusion, there are limited data about follow-up colonoscopy after a CT diagnosis of acute diverticulitis, and the pooled prevalence of colorectal cancer in a small number of patients is only slightly higher than the calculated prevalence of colorectal cancer in a population of comparable age. The available studies did not specifically examine CT or clinical findings that would predict or exclude the possibility of colorectal cancer. On the basis of these data, we question whether the routine recommendation of follow-up colonoscopy in this situation to exclude colon cancer is clinically warranted and cost effective or whether more refined criteria should be developed. A larger and preferably prospective study is necessary to determine the validity of the recommendation for colonoscopic follow-up after a CT diagnosis of acute diverticulitis. In either case, whether age-appropriate colorectal cancer screening has been performed should be reviewed after a diagnosis of acute diverticulitis.
Advance in Knowledge.
• On the basis of a limited number of published studies, the pooled prevalence of colorectal cancer after a CT diagnosis of acute diverticulitis is 2.1%.
Implication for Patient Care.
• There are limited data supporting routine follow-up colonoscopy after a CT diagnosis of acute diverticulitis; more refined criteria for recommending colonoscopy should be developed.
Disclosures of Potential Conflicts of Interest: V.F.S. No potential conflicts of interest to disclose. F.V. No potential conflicts of interest to disclose. J.N. No potential conflicts of interest to disclose. A.C.W. No potential conflicts of interest to disclose.
Acknowledgments
The authors thank Gloria Won, MLIS, for her assistance with the literature search.
Footnotes
Received September 1, 2011; revision requested November 1; revision received November 11; accepted December 8; final version accepted December 20.
Funding: This research was supported by the National Institutes of Health (NIH/NCRR/OD UCSF-CTSI grant KL2 RR024130).
Contents are solely the responsibility of the authors and do not necessarily represent the official views of the National Institutes of Health. This is a career development award without any direct role in design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the manuscript.
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