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Original Research |
1 All authors: Department of Radiology, Hospital Universitario Dr. Peset, 90 Gaspar Aguilar Ave., Valencia 46017, Spain.
Received December 2, 2004;
accepted after revision February 14, 2005.
Address correspondence to T. Ripollés
(ripolles_tom{at}gva.es).
Abstract
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MATERIALS AND METHODS. Analysis of the sonographic examinations was performed over 5 years in 190 patients with an established diagnosis of Crohn's disease. Data analyzed were as follows: visualization of the appendix; thickness and color Doppler signal (grade 0, 1, or 2) of the appendix and adjacent intestinal loop (cecum, terminal ileum, or both); involvement of other intestinal segments; and abscesses. The findings were compared with those of 49 consecutive patients with sonographic findings of acute appendicitis.
RESULTS. Thirty-nine patients with Crohn's disease (21%) had appendicular involvement. All but one patient showed thickening of the terminal ileum, and 46% of patients also showed thickening of the cecum. The thickness of the ileum was more than 5 mm (only the anterior wall) in 64% of patients. Appendicular hyperemia was seen in 72% of patients. Involvement of other segments was seen in 23 patients (59%) and adjacent abscesses in six (15%). Irregular thickness of the submucosa was seen in nine cases (23%) and fibrofatty proliferation in 19 (49%). In patients with ileocecal regional disease, ileum thickness of more than 5 mm and visible color in the ileum were the most valuable signs, both for the diagnosis of Crohn's disease and to differentiate it from acute appendicitis (positive predictive value, 96%; negative predictive value, 74%).
CONCLUSION. Appendicular involvement in Crohn's disease is a relatively frequent event (21%). Sonography and color Doppler sonography may be useful for differentiating Crohn's disease with appendicular involvement from acute appendicitis.
Keywords: appendicitis • appendix • Crohn's disease • Doppler studies • sonography
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Our aim was twofold: first, to analyze sonography findings (both gray-scale and color Doppler sonography) in patients with appendicular involvement in Crohn's disease and, second, to determine whether sonographic differences exist between Crohn's disease of the ileocecal region and acute appendicitis.
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The sonographic studies included in this study were performed by experienced sonographers during regular working hours on weekdays. The sonographic examinations were performed after the patient had fasted. The examinations were performed on a Sonolayer SSH-140A or a PowerVision 5000 scanner (Toshiba) using a 3.5-MHz convex or 5- to 10-MHz linear transducer. The graded compression technique was used. Color Doppler flow parameters were optimized for maximal sensitivity using a special preset designed for the detection of low-velocity flow in the bowel wall (filter at low setting, 50 Hz; lowest velocity scale, 2 cm/sec).
For each affected segment, the following sonographic features were assessed: bowel wall thickness; stratification of the intestinal wall (normal or absent); and presence of abscesses, fistulas, or signs of bowel luminal occlusion. Fibrofatty proliferation was also evaluated when a segment of abnormal small bowel was detected. The presence of color Doppler flow was determined in abnormal loops of bowel in all patients. The appendix was also evaluated, including its thickness and wall vascularization. A standard questionnaire was completed after each sonographic examination.
An intestinal segment was considered abnormal if the anterior bowel wall was at least 3 mm thick (measuring the thickness of the anterior wall from the outer wall to the mucosa-gas surface) [6, 7]. The terminal ileum was arbitrarily defined as the last 5-7 cm of ileum. Color Doppler flow was considered present when color pixels persisted throughout the observation period. Color Doppler flow was always confirmed by obtaining an arterial or venous signal at the location of the color pixel. Color Doppler flow was subjectively graded as absent (grade 0), barely visible (grade 1), or readily visible (grade 2) [7, 8]. An appendix larger than 6 mm with or without Doppler signal was always considered abnormal. Cases with a 5- to 6-mm appendix with color Doppler signal were also included among the abnormal cases [9].
The sonographic findings analyzed were prospectively obtained from the original questionnaire completed after each sonographic examination. The hard-copy images were reviewed only to provide some additional sonographic characteristics—that is, the length of involvement or the presence of marked and irregular thickening of the submucosal layer. The sonography findings were assessed by consensus between two expert radiologists.
During the reviewed period (1997-2001), 190 patients with established Crohn's disease underwent abdominal sonography. In 39 (21%) of the 190 patients examined, sonography showed abnormal findings for the appendix: 36 were larger than 6 mm and three were smaller than 6 mm but showed Doppler signal. The study group comprised these 39 patients (16 females, 23 males; age range, 15-54 years; mean age, 27.9 ± 10 [SD] years). Four patients presented in the emergency department with right lower quadrant pain, and the remaining 35 patients were seen in the outpatient clinic. During the time of this review, 24 of the 39 patients had undergone more than one sonographic examination; for those patients, only the first sonography examination was used. The diagnosis of Crohn's disease was established on the basis of surgical and pathologic findings in three patients, barium study or colonoscopic biopsy in 169 patients, or both in 21 patients. An attempt was made to correlate the degree of color Doppler flow of the ileum and clinical activity of the disease. The clinical records of the patients with Crohn's disease were reviewed to obtain a Crohn's Disease Activity Index (CDAI) value recorded within 5 days of the sonographic evaluation.
The sonographic findings in the ileocecal region in patients with Crohn's disease (thickness and vascularization of the appendix, terminal ileum, and cecum) were compared with those in a control group of 49 consecutive patients with surgically and histologically proven acute appendicitis. The comparison group comprised 25 females and 24 males who ranged in age from 7 to 79 years and had a mean age of 32.2 ± 18.9 years.
Statistical Analysis
Basic descriptive statistics, including the mean and SD for continuous
variables, and the absolute frequency and percentage for discrete variables
were used to characterize the study patients.
Later, the variables observed in each group of patients (group with Crohn's disease involving the appendix and group with acute appendicitis) were compared to identify statistically significant differences. For univariate analysis, the Student's t test or the Mann-Whitney U test (if the sample size was fewer than 30 or if the variables were not normally distributed) was applied for comparing continuous variables. The association between categoric variables was tested using either the Fisher's exact test if the expected number of observations in one or more cells of the table was fewer than five or the chisquare test otherwise. A p value of less than 0.05 was considered to indicate a statistically significant difference. In addition, we attempted to identify combinations of sonographic findings that provided the best specificity or positive predictive value (PPV).
Finally, a multivariate nonconditional logistic regression model was developed. The association measure was the odds ratio, with calculation of the corresponding 95% confidence limits. A statistical package (version 9.0, Statistical Package for the Social Sciences) was used.
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The other intestinal segments involved were the ileum in seven patients, ascending colon in two, and other colonic segments in eight; pancolitis was seen in five patients. The only patient with an ileum of normal thickness had pancolitis.
There was a statistically significant correlation between the appendix thickness and the ileum thickness (p = 0.002). Color in the appendiceal wall was also statistically associated with ileum (p = 0.001) and cecum (p = 0.018) color Doppler flow. The mean size of abscesses was 6.8 cm (range, 3-15 cm).
Twenty-nine patients had a CDAI value calculated: 22 (76%) had a CDAI value of greater than 150, which is consistent with clinical activity. There was a significant correlation between color in the ileum wall and clinical disease activity (i.e., CDAI value) (p = 0.007), with 95% sensitivity and 57% specificity (21 true-positives [patients with hyperemia in the ileum walls and CDAI > 150], four true-negatives [patients without color in the ileum walls and CDAI < 150], three false-positives, one false-negative).
The sonographic appearance of the ileocecal region of 39 patients with Crohn's disease involving the appendix, regardless of sonographic involvement of other intestinal segments, was compared with the findings of 49 patients with acute appendicitis. Comparative sonographic findings are summarized in Table 2.
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There were significant differences between the two diseases regarding thickness of the appendix (thicker in patients with acute appendicitis) and the thickness of the ileum and cecum (thicker in those with Crohn's disease). For statistical analysis, ileum thickness was dichotomized into two groups: 5 mm or less and greater than 5 mm. When ileum thickness was greater than 5 mm, a diagnosis of Crohn's disease could be made with a specificity of 94% (46/49) and a PPV of 89% (25/28).
Significant differences between the two diseases were also found by using ileum and cecum wall thickening in combination (p = 0.003). Isolated ileal involvement was more frequent in patients with Crohn's disease (19 cases, 49%) than in acute appendicitis (four cases, 8%) (PPV of 83% for a diagnosis of Crohn's disease). Isolated cecal involvement was seen in 18 patients (37%) with acute appendicitis and only in one patient (2%) with Crohn's disease. The negative predictive value (NPV) for a diagnosis of Crohn's disease was 94%. Combined cecal and ileal involvement was seen in 19 patients (49%) with Crohn's disease and in seven (14%) with acute appendicitis.
Regarding color Doppler flow, significant differences between the two diseases were found only in the ileum (Table 1). Identifiable Doppler ileum wall flow was seen in 33 patients (85%) with Crohn's disease (Figs. 3A, 3B, 4A, and 4B), and absence of color Doppler signal in the ileum was seen in 41 patients (84%) with acute appendicitis (Figs. 5A and 5B). The sensitivity was 85% (33/39); specificity, 84% (41/49); PPV, 80% (33/41); and NPV, 87% (41/47).
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Ileum of 5 mm or less with an absence of color was a significant predictor of acute appendicitis. The PPV and NPV of an ileum of 5 mm or less and the absence of color Doppler flow for the differentiation of acute appendicitis from Crohn's disease were 93% (39/42) and 78% (36/46), respectively; this combination was seen in only three of 39 patients with Crohn's disease.
Of the 17 patients with Crohn's disease and ileum greater than 5 mm, absence of color, or both (Table 3), only four had isolated involvement of the ileocecal region, whereas the remaining patients had involvement of multiple segments.
Predictors
Table 4 shows the results of
multivariate logistic regression analysis of each parameter for
differentiating Crohn's disease with appendiceal involvement from acute
appendicitis. The most significant predictors of Crohn's disease were ileum
thickness greater than 5 mm and color (grade 1 or 2) in the ileum wall.
Appendix color (grade 2) was the only variable significantly associated with
the diagnosis of acute appendicitis. The other sonographic variables were
nonsignificant.
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The probability of Crohn's disease was almost 35-fold greater when readily visible color Doppler signal (grade 2) was seen in the ileal wall, fourfold greater in the presence of barely visible signal (grade 1) in the ileum, and fivefold greater in the presence of an ileum greater than 5 mm. The probability of acute appendicitis was almost 16-fold greater in the presence of color readily visible (grade 2) in the appendix.
Follow-Up
The patients with Crohn's disease were followed between 6 and 80 months
(mean, 52 ± 21.3 months) with review of medical records and
surgical-pathologic report when available. No patients were lost to
follow-up.
During this period, six patients underwent surgery. The interval between sonographic examinations and surgery ranged between 15 and 370 days (mean, 192 ± 170 days). Histologic proof of Crohn's disease of the ileum, cecum, and appendix was obtained in all patients. One patient had surgery on an emergency basis. Another had an abscess drained. There were no significant differences in the sonography findings (color and thickness of the appendix, ileum, and cecum) among patients with Crohn's disease who underwent surgery and those who did not.
Forty-six of 49 patients with acute appendicitis had emergency surgery. Three patients had delayed surgery due to an appendiceal inflammatory mass.
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In our series, appendiceal involvement in Crohn's disease was always associated with segmental thickening of the terminal part of the ileum, cecum, or both. The terminal ileum was involved in 38 patients (97%), in association with thickening of the cecum in 19 patients (49%). Only one patient (3%) had isolated cecal wall thickening. Previous descriptions (small series or pictorial reviews) have reported that in cases of Crohn's disease with appendiceal involvement, mural thickening of the ileum or cecum should be severe [1, 4, 10]. On the basis of our results, appendicular involvement in Crohn's disease can be detected with sonography in many patients who present with only mild ileocecal changes, including many patients with a normal cecum. Severe wall thickening was seen in the terminal ileum in 64% of patients, but in the cecum in only 28% of patients.
In our series, other intestinal segments were frequently associated. Only 16 (41%) of 39 patients with Crohn's disease showed abnormal sonographic findings confined to the ileocecal region, whereas 59% of patients had wall thickening involving other intestinal segments.
In the opinion of Sarrazin and Wilson [5], reactive thickening of the appendix due to inflammation of active ileocecal Crohn's disease should show color Doppler flow in the terminal ileum or cecum, but not in the appendix. However, in our series color Doppler flow in the appendiceal wall was seen in 72% of patients with Crohn's disease and sonographic appendiceal involvement. The majority of cases with thickening of the ileum or cecum also showed increased flow in the intestinal wall. We found a statistically significant association between color in the appendiceal wall and the color Doppler flow of the ileum or cecum. In patients with active Crohn's disease, there is increased vascularity in the wall of the involved intestinal segments that can be seen with color Doppler imaging [12, 13]. Most of our patients had active disease (CDAI account for > 150), which would the high percentage of hyperemia found in the intestinal wall and the appendix. Indeed, it is possible that in a group of patients with less inflammatory activity the percentage of cases with color Doppler flow in the intestinal wall would be diminished.
We did not find any case of Crohn's disease with isolated appendicular disease. Granulomatous appendicitis with no extraappendiceal gastrointestinal tract involvement is a rare condition discovered incidentally in patients with clinical presentation of acute appendicitis. Although previously considered a form of Crohn's disease isolated to the appendix, idiopathic granulomatous appendicitis is now believed by many authors [11, 14] to be an entity distinct from Crohn's disease. Inclusion criteria of our study, i.e., only patients with an established diagnosis of Crohn's disease, explain the absence of these cases in our series.
In many hospitals sonography is the first imaging examination to evaluate patients with right lower quadrant pain and suspected acute appendicitis. Most patients with Crohn's disease do not have appendicular involvement; therefore, it should be easy to distinguish them from patients with acute appendicitis in an emergency setting. However, newly diagnosed cases of Crohn's disease with appendicular involvement are the difficult ones to differentiate from cases of acute appendicitis. The importance of distinguishing both entities is obvious: Acute appendicitis usually requires surgery, whereas Crohn's disease does not. To our knowledge, the similarities and differences in the sonographic appearances between these two conditions have not been previously addressed in a comparative analysis.
Sonographic involvement of intestinal segments outside the ileocecal region (56% in our study) is an obvious specific feature of Crohn's disease when compared with acute appendicitis. Other specific features of Crohn's disease that were not present in acute appendicitis were irregular thickening of the submucosal layer of the terminal ileum and fibrofatty proliferation of the mesentery around the inflamed terminal ileum. Irregular thickening of the submucosal layer is a sonographic finding that has been described in Crohn's disease [15], although it can also be seen in varied acute gastrointestinal abnormalities that course with submucosal edema or hemorrhage [16]. None of our patients who had acute appendicitis associated with ileal wall thickening had this finding. On the other hand, patients with acute appendicitis may show inflammation of the fat surrounding the appendix, whereas the fibrofatty proliferation characteristic of Crohn's disease is always situated around the bowel involved [5, 15, 17].
In cases in which appendicular involvement in Crohn's disease is limited to the ileocecal region, the results of our study showed that despite some overlap a few sonographic features were useful for differentiating Crohn's disease involving the appendix from acute appendicitis. According to the results of our multivariate logistic regression analysis, thickness of the ileum greater than 5 mm and color Doppler flow in the terminal ileum were the most valuable sonographic findings with which to differentiate Crohn's disease involving the appendix from acute appendicitis, with a PPV and NPV as high as 96% and 74%, respectively. Fifty-six percent of patients with Crohn's disease showed these sonographic features compared with only 2% of patients with acute appendicitis. The combination of these findings—ileum thickness greater than 5 mm and color Doppler flow—is therefore a significant predictor of Crohn's disease and virtually excludes acute appendicitis. Conversely, an ileum of 5 mm or less with no parietal color flow strongly suggests acute appendicitis. As far as statistical analysis results, we prefer to obtain a high specificity because false-positive diagnosis of Crohn's disease in this setting can lead to serious consequences. It is known that, except in cases with extensive periappendiceal phlegmon, patients with appendicitis usually undergo immediate appendectomy to try to decrease the perforation rate.
Thickening of the ileum and cecum may be seen in both diseases, but when the thickening is severe (> 5 mm), it is suggestive of Crohn's disease, with a PPV of 90%. Isolated thickening of the ileum suggests Crohn's disease; conversely, a normal ileum almost excludes it. On the other hand, isolated thickening of the cecum suggests acute appendicitis (NPV of 94% for the diagnosis of Crohn's disease). Cecal wall thickening is a feature that has been described extensively in the diagnosis of acute appendicitis using CT. In our series, cecal wall thickening of greater than 5 mm was detected on sonography in 14% of patients with acute appendicitis, a percentage less than that (24%) reported by Kessler et al. [18].
Hyperemia in the wall of the appendix shown on color Doppler images has been considered a specific sign for acute appendicitis [9, 18, 19]. Previous reports have shown that most patients with acute appendicitis (87-88%) have color in the appendiceal wall on color Doppler sonographic images [9, 19], which is comparable with our results (88%). In our series, most patients with Crohn's disease and appendicular involvement (73%) also showed hyperemia in the appendix, indicating that appendiceal hyperemia may be seen in other diseases besides acute appendicitis. Despite this finding, on the basis of the results of logistic regression, the evaluation of color Doppler flow of the appendix can aid in distinguishing between the two diseases: Appendiceal hyperemia—without color Doppler flow in the ileum wall—suggests acute appendicitis.
There are several limitations to our study. First, surgical proof was not obtained in most of our patients with Crohn's disease. Only six patients underwent surgery, with histologic confirmation of involvement of the appendix in all cases. There were no significant differences regarding sonographic features of patients who underwent surgery and those who did not in our series; this fact indicates involvement of the appendix in the remaining cases as well. However, according to previous articles, the normal appendix may measure more than 6 mm, so some of our patients with an appendix of 6 mm or more could have been normal [20]. On the other hand, appendicitis is known to occasionally resolve spontaneously, so we cannot be sure that some patients were actually cases of primary acute appendicitis. Nevertheless, the aim of our study was to describe the sonographic features of Crohn's disease involving the appendix and to analyze the sonographic differences between thickening of the appendix secondary to Crohn's disease and acute appendicitis. We did not attempt to determine the sensitivity or specificity of sonography in the diagnosis of involvement of the appendix in Crohn's disease.
A second limitation is the fact that this study is retrospective, with data collected over a period of 5 years and involving sonography studies performed by different radiologists. This could imply the existence of variability in the evaluation of the sonographic findings, particularly regarding the parietal vascularization determined by color Doppler flow. We believe that this limitation is unavoidable because of the relative rarity of this entity and the need to collect a sufficient number of cases to achieve statistical significance.
The last limitation consists of a possible bias in patients with Crohn's disease included in the study. Most of our patients had inflammatory activity according to clinical criteria (CDAI > 150). In patients with active Crohn's disease, an increased vascularity and thickness of the intestinal loop have been described [12, 13]. Patients with less inflammatory activity would probably show lower grades of color and thickening of the intestinal loop, which would appear more similar to the sonographic findings of acute appendicitis, making it difficult to distinguish one from the other.
Other possible diagnoses were not considered in this article. Secondary enlargement of the appendix can be caused by cecal cancer or other inflammatory bowel diseases of the ileocecal region (e.g., diverticulitis, tuberculosis, typhlitis).
In many institutions, CT is the first imaging technique for evaluating both patients with right lower quadrant pain and those with Crohn's disease. On CT scans, confusion can also exist between acute appendicitis and appendicular involvement by Crohn's disease. In our opinion, the results of this study could also be of value in CT studies.
In conclusion, sonographic appendiceal involvement in Crohn's disease is a relatively common feature (21%) and is usually associated with thickening of the ileum, cecum, or both. Most patients have appendiceal and bowel wall color Doppler flow. On the basis of our results, sonography may be useful for differentiating Crohn's disease involving the appendix from acute appendicitis. Involvement of other intestinal segments is a frequent sonographic finding in patients with Crohn's disease. In cases with isolated ileocecal region involvement, terminal ileum thickness of greater than 5 mm and color Doppler flow in the ileum are the most valuable sonographic findings to differentiate Crohn's disease from acute appendicitis. Other findings, including thickening of the submucosal layer of the ileum wall and fibrofatty proliferation, can provide supplementary information.
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