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British Journal of Radiology (2004) 77, 917-921
© 2004 British Institute of Radiology
doi: 10.1259/bjr/18038687
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Full Paper

Focal bowel wall changes detected with colour Doppler ultrasound: diagnostic value in acute non-diverticular diseases of the colon

E M Danse, MD , PhD1, J Jamart, MD, MSc2, P Hoang, MD, PhD3, P F Laterre, MD4, A Kartheuser, MD, PhD5 and B E Van Beers, MD, PhD1

1 Department of Radiology, Université Catholique de Louvain, St-Luc University Hospital, Avenue Hippocrate 10, B-1200 Brussels, 2 Center for Biostatistics and Medical Documentation, Mont-Godinne University Hospital, Avenue Therasse 1, B-5530 Yvoir, 3 Department of Internal Medicine, St-Luc University Hospital, Avenue Hippocrate 10, B-1200 Brussels, 4 Department of Intensive Care and Emergency Medicine, St-Luc University Hospital, Avenue Hippocrate 10, B-1200 Brussels and 5 Department of Surgery, St-Luc University Hospital, Avenue Hippocrate 10, B-1200 Brussels, Belgium


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Discussion
 References
 
We performed a study to determine if colour Doppler findings may help to identify the cause of wall thickening in acute non-diverticular diseases of the colon. The study group included 66 patients admitted to the emergency department with a final diagnosis of infectious colitis (n=23), inflammatory colitis (n=10), ischaemic colitis (n=23) and malignant tumours (n=10). The following ultrasound features were assessed: maximal wall thickness, wall stratification, arterial flow in the colonic wall and arteriolar resistive index. Higher values of wall thickness were observed in malignant tumour (18.2±6.2 mm, p<0.001). Moderately thickened wall (6.6±1.3 mm, p≤0.06), preserved stratification (90% versus 46% in the remainder of the study population) and lower resistive index (0.51±0.10, p≤0.05) were significantly related to inflammatory colitis. Absence of arterial flow was more frequently observed in ischaemia (43% versus 12% in the remainder of the study population). In conclusion, despite some overlap, both ultrasound and colour Doppler features are helpful in the differential diagnosis of colonic thickening related to non-diverticular colonic lesions.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Discussion
 References
 
Ultrasound (US) can be used in the diagnosis and the follow-up of various gastrointestinal diseases [1–6]. Both diverticulitis and non-diverticular lesions can cause thickening of the colonic wall detectable with US [6, 7]. The US findings of colonic diverticulitis have been well described and this diagnosis is often easily performed with US when the inflamed diverticulum is observed [8]. However, reports evaluating the role of colour Doppler analysis of the colonic wall for differentiating between non-diverticular colonic disorders are sparse [9–13]. Truong et al [7] assessed the US findings of colonic lesions but did not use colour Doppler. Shirahama et al [13] have demonstrated promising results of colour Doppler analysis of the gut wall, in a study including small bowel and colonic diseases. The aim of our paper was to evaluate whether US combined with colour Doppler features can identify the cause of wall thickening in acute non-diverticular diseases of the colon.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Discussion
 References
 
In our institution, colour Doppler US of the abdomen is used as the initial imaging method in patients with non-specific acute or chronic abdominal pain. We retrospectively reviewed the clinical and US findings of adult patients admitted with acute abdominal pain, and referred for US. The clinical database showed that during a 5 year period, 66 patients with a diagnosis of acute colonic disease other than diverticulitis or appendicitis had a thickened colonic wall at colour Doppler US. All the patients were evaluated by the same radiologist (ED) in charge of the radiological unit of the emergency department These patients formed the study group that included 32 men and 34 women (age range: 17–95 years, median: 60 years). 23 patients had acute infectious colitis (including five patients with pseudomembranous colitis and two with neutropenic typhlitis), 10 had inflammatory colitis (including nine with Crohn's colitis and one with ulcerative colitis), 23 had ischaemic colitis and 10 malignant tumours including nine colonic adenocarcinomas and one intramural ovarian metastasis. The final diagnosis was obtained by colonoscopy with biopsy (n=28), surgery (n=22), clinical history and follow-up (n=10), stools cultures (n=5) and Clostridium difficile titres (n=1).

The patients were evaluated with commercially available US machines, equipped with low frequency sector or convex probes ranging from 3 MHz to 3.5 MHz and linear probes with frequencies from 5 MHz to 10 MHz. All the patients underwent a standardized US examination starting by scanning the abdomen with the low frequency probes, in order to assess the main abdominal vessels (the aorta, portal, splenic and mesenteric veins and arteries), the liver, biliary tract, gallbladder, kidneys, spleen and pancreas. A detailed study of the colon was obtained with the high frequency probes. The analysis of the colon was made with the technique of Pradel et al [14] beginning in the left iliac fossa, where the sigmoid colon can be easily identified. The whole length of the colon including the ileocolonic junction was scanned. The colonic wall was evaluated with graded compression [1, 5]. The thickness of the anterior wall of the colon was measured as the distance between the inner hyperechoic line created by the interface of the luminal content and the superficial mucosa and the outer hyperechoic line related to the serosal layer of the colic wall. The colic wall was considered to be thickened when it was greater than 4 mm. It was considered stratified when the mucosa, submucosa and muscularis propria were visualized as separate layers (Figure 1Go). The parietal vascularization was studied by standardized colour and duplex Doppler sampling. Controlled parameters included a filter for low volume flow, lowest pulse repetition frequency without aliasing and maximal gain without background noise. Colour Doppler flow was noted present when coloured pixels were identified in the thickened wall throughout the observation period. Duplex Doppler samples oriented on the main coloured pixels were used to differentiate between arterial and venous signals. The resistive index (peak systolic velocity value – end diastolic velocity value/peak systolic velocity value) was calculated on the spectral waveform when arteriolar flow was observed. The resistive index was automatically calculated during the examination by using dedicated software.



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  		Figure 1. 68-year-old man with infectious colitis. Transverse ultrasound shows colonic wall thickening with preserved stratification. Interface between lumen and mucosa appears hyperechoic; mucosa is hypoechoic (arrowhead); submucosa, hyperechoic (asterisk) and muscularis propria, hypoechoic (arrow).

 
Numerical variables are expressed as mean±standard deviation and were compared by the Wilcoxon rank sum test. Categorical variables were studied by the chi square test. A logistic regression with backward selection of variables by the likelihood ratio test was used to assess the value of the numerical variables namely the wall thickness and the resistive index on the various diagnoses. For these variables, receiver operating characteristic (ROC) curves were constructed by maximum likelihood estimation under the binormal model with the LABROC1 program (C.E.Metz, University of Chicago, Chicago, IL). Other analyses were performed with the SPSS software (SPSS Inc., Chicago, IL). All statistical tests are two-tailed.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Discussion
 References
 
The results are listed in Table 1Go. The statistical analysis showed that the colonic wall was larger in the malignant tumours than in the other conditions (p<0.001 versus inflammation, ischaemia and infection). In contrast, the colon wall thickness was lower in inflammation than in the other diseases (p=0.057 versus infection, p=0.004 versus ischaemia, and p<0.001 versus malignancy) (Figure 2aGo). Stratification was more frequently preserved in inflammation than in ischaemia (p=0.051) and malignancy (p=0.005). Absence of identifiable arterial flow in the colonic wall was significantly more frequent in ischaemia than in inflammation (p=0.025) and infection (p=0.047). The resistive index was significantly lower in inflammation than in infection (p=0.039), ischaemia (p=0.049) and malignancy (p=0.012) (Figure 2bGo).


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  		Table 1. Comparison of colour Doppler ultrasound features

 


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  		Figure 2. Box plots of group parameters in which boundary of boxes closest to zero indicates 25th percentile, line within boxes marks median, and boundary of boxes farthest from zero indicates 75th percentile. Errors bars below and above boxes indicate 10th and 90th percentiles. Outliers are represented as individuals points. Graphs showing box plots of (a) wall thickness, and (b) resistive index. Malignancy is significantly related to increased wall thickness (p<0.001), and inflammation is related to lower values of resistive index compared with other groups (p≤0.05).

 
The logistic regression analysis selected the wall thickness, but not the resistive index, for predicting malignancy while both parameters were significant predictors of inflammation. The ROC curve of the wall thickness in the diagnosis of malignancy had an area under the curve of 0.959±0.024 (Figure 3Go). A cut off value of 12 mm thickness gave a sensitivity and specificity of 90% for the diagnosis of colonic tumour. In the diagnosis of inflammatory colitis, the ROC curves had areas of 0.800±0.059 when the wall thickness was considered, 0.763±0.078 when the resistive index was considered, and 0.840±0.053 when both parameters were considered together (Figure 4Go).



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  		Figure 3. Receiver operating characteristic curve of wall thickness in diagnosis of malignancy has area under curve of 0.959±0.024.

 


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  		Figure 4. Composite receiver operating characteristic curves of wall thickness (C1), resistive index (C2), and both parameters (C3) for diagnosing inflammation show larger area under curve when both parameters are considered together.

 

   Discussion
Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
References
 
We assessed whether colour Doppler US features are helpful in identifying the cause of colonic wall thickening. High colonic wall thickness was suggestive of malignant tumours. A cut off value of 12 mm had a sensitivity and specificity of 90%. This is in accordance with previously published values of 10–20 mm in colonic tumours [7, 15–19]. In addition, loss of wall stratification was observed in 80% of colonic tumours in our series and in 85% in a previous study published by Truong et al [7] (Figure 5Go). Loss of stratification can be explained by the invasion of the deep wall layers by the tumours [7, 15, 17, 20]. The observed high wall thickness and loss of stratification underscore the fact that the colonic tumours are often large when they become symptomatic. We observed preserved wall stratification in two of the 10 malignancies; similar results were noted in the series of Truong et al [7]. This illustrates that US can be used to demonstrate the invasion of the deep layers of the colon by tumours [20].



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  		Figure 5. 69-year-old woman with colonic carcinoma. Transverse ultrasound shows hypoechoic and irregular thickening of colonic wall, without stratification.

 
Moderate colonic thickening, preservation of stratification and low resistive index were suggestive of inflammatory colitis in our study (Figure 6Go). It has been reported that increased wall thickness and disappearance of stratification were more frequent in Crohn's disease than in ulcerative colitis, but the data often overlapped [7, 21, 22]. The precise measurement of the wall thickness is not considered by everybody as crucial for the diagnosis and staging of inflammatory bowel disease [23]. More recently, preserved wall stratification has been reported as an indicator of the acute forms of inflammatory bowel diseases [24–27]. This is in accordance with the findings in our series where the majority of patients were admitted to the emergency department for acute symptoms. Wall vascularization has also been reported as a useful sign for the assessment of the activity of inflammatory diseases [28–30]. Our results show that acute inflammatory colitis is associated with significantly lower values of the resistive index than other colonic diseases and that the diagnosis of inflammatory colitis is more accurate when low values of both wall thickness and resistive index are observed.



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  		Figure 6. 21-year-old woman with Crohn's colitis. Transverse Doppler ultrasound of the caecum (arrows) demonstrates increased mural flow and low value of mural resistive index.

 
As was shown in our series and in previous studies, infection of the colon causes variable wall thickening [2, 14, 18, 31, 32]. Higher values are more frequently observed in severe colitides, such as pseudomembranous or neutropenic colitides [16, 33–35]. Disappearance of stratification, noted in 44% of our cases, and increased mural flow can be noted in infectious colitis, mimicking Crohn's disease [36].

Ischaemic colitis was characterized by greater increases in wall thickness compared with that seen with inflammation, more frequent loss of wall stratification and absence of flow on colour Doppler (Figure 7Go). It has been reported that the increased wall thickness seen with ischaemia may be secondary to submucosal haemorrhage following reperfusion [16, 37, 38].



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  		Figure 7. 75-year-old woman with ischaemic colitis. Doppler ultrasound shows hypoechoic thickening of the colon with absence of mural flow (arrows).

 
Loss of stratification is related to the duration of ischaemia as observed by Cheung et al [39]. Absence of flow is suggestive of ischaemia [9–13, 25]. However, intramural flow may be present in transient ischaemic colitis [40] and was observed in 57% of the patients in this series. This finding was also reported by Teefey et al in 50% of patients with wall thickening due to ischaemia [9].

Our study has some limitations. The length of colonic wall thickening, features of pericolic structure, and small bowel involvement were not evaluated but these features have been assessed previously and contribute to the diagnosis of digestive diseases particularly for Crohn's disease, diverticulitis and ischaemic colitis [7]. Our investigation focused on non-diverticular colonic diseases producing wall thickening. The diagnosis of colonic diverticulitis is often easily made when the inflamed diverticulum is shown at US. Another limitation of our study is related to the fact that the detailed scanning protocol may be difficult to perform without a radiologist subspecialized in emergency radiology and practicing in the emergency department.

With CT, the degree of luminal distension can affect the colonic wall thickness, as observed by Wiesner et al [41]. In our study, this effect was not evaluated.

Our study was based on a retrospective analysis of US findings including the presence or absence of colonic flow. A more precise quantification of the mural flow was not available.

In conclusion, the US features observed in colonic wall thickening caused by acute non-diverticular diseases may overlap. Nevertheless, some findings may suggest the final diagnosis. Highly thickened wall is suggestive of malignancy. Inflammation is related to moderate thickening with preserved stratification and low value of the resistive index. Absence of identifiable flow with colour Doppler US is suggestive of ischaemic colitis.

Received for publication November 20, 2003. Revision received April 30, 2004. Accepted for publication June 29, 2004.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 References
 

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This Article
Right arrow Abstract Freely available
Right arrow Figures Only
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Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
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Citing Articles
Right arrow Citing Articles via Google Scholar
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Right arrow Articles by Danse, E M
Right arrow Articles by Van Beers, B E
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PubMed
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Right arrow Articles by Danse, E M
Right arrow Articles by Van Beers, B E

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