Role of contrast-enhanced ultrasound in evaluation of the bowel
Contrast-enhanced ultrasound (CEUS) of the gastrointestinal tract provides vascular information helpful for characterizing masses and other pathologies in and around the bowel, similar to contrast applications in other solid organs. However, the use of microbubble contrast agents for the bowel provides additional unique contributions as it gives both subjective and objective information about mural and mesenteric blood flow, invaluable for the determination of disease activity in those many patients affected by inflammatory bowel disease (IBD). IBD is a lifelong chronic disease and has its peak age of onset in adolescence or young adult life. Today, we have moved away from treating patient’s symptoms and strive instead to alter the course of disease by obtaining mucosal healing. Expensive and aggressive biologic therapies and lack of agreement of patient’s symptoms with their disease activity and complications necessitate frequent imaging surveillance, which must be safe, readily available, inexpensive, and effective. Ultrasound with the benefit of contrast enhancement meets these requirements and is shown in meta-analysis to be equivalent to CT and MRI scans for these indications.
KeywordsContrast enhanced ultrasound Ultrasound Bowel Inflammatory bowel disease Gastrointestinal
Sonographic evaluation of the bowel has become one of the most valuable advancements of ultrasound in the past decade especially for patients with inflammatory bowel disease (IBD) who require frequent monitoring of their inflammatory activity due to its natural fluctuating course and the current use of biologic therapies . Multiple studies have shown the accuracy of grayscale ultrasound (US) for determination of disease extent and activity [1, 2, 3, 4, 5]. Although, bowel wall thickness is the most reliable feature reflecting inflammation in the bowel wall, some patients with quiescent disease continue to show bowel wall thickening in the absence of active inflammation [5, 6, 7]. In addition, sensitive detection of response to therapy may require more than just gross morphologic assessment. Therefore, detection and evaluation of vascular flow is an important factor in the diagnosis of bowel disease.
It is known that active inflammation is accompanied by neoangiogenesis of the bowel wall and vascularization of the adjacent mesenterium [8, 9, 10]. Mural blood flow detected with color Doppler imaging (CDI) has been viewed for many years as a reflection of active inflammation, allowing for monitoring of disease activity [9, 11]. On the other hand, if color Doppler signal is absent, this may suggest inactive disease in the case of IBD  or ischemia in the setting of acute or chronic abdominal pain .
Current state of the art ultrasound equipment provides sensitive Doppler technology which can show mural and mesenteric blood flow with relative ease [11, 14]. However, CDI reflects large blood vessels with fast flow [11, 12, 15]. Signals may be difficult to detect in large patients, in those with inherently weak Doppler signals, and in bowel loops located deep within the abdomen or pelvis. However, the most significant weakness of CDI is its inability to show blood flow at the capillary or perfusion level, important for determination of disease activity . Therefore, a confident evaluation of the bowel with only grayscale ultrasound and CDI may be deficient.
As with other cross-sectional modalities, the introduction of contrast agents for ultrasound has improved the assessment of the bowel vasculature. CEUS is performed with microbubble contrast agents which provide subjective and objective parameters that reflect inflammation by showing enhancement of the bowel wall and mesentery. Studies have shown a direct correlation between level of bowel wall enhancement and active inflammatory disease on pathology [16, 17, 18, 19]. In addition, they enable the creation of time–intensity curves from which quantification of bowel wall enhancement will reflect the bowel fractional blood volume, the blood flow, and the transit time. Based on this quantification analysis, the presence and degree of inflammation can be objectively assessed and followed over time. This is particularly important for evaluation of treatment response by comparing quantification values over a series of studies.
Additionally, CEUS can be used for characterization of masses in the bowel wall or adjacent mesenterium. This resolves dilemmas which frequently arise during grayscale evaluation as colonic content, inflammatory polyp, and neoplasm can all overlap in appearance. Further, CEUS is particularly important in the differentiation of inflammatory masses as either phlegmon or abscess, as their treatment would vary.
In our experience, the addition of CEUS for assessment of bowel pathology has significantly improved our ability to detect, evaluate and objectively quantify the presence of bowel inflammation and its complications. The non-ionizing nature of this technique makes ultrasound a desirable alternative in the frequently young patient with IBD who has a high demand for imaging throughout the chronic course of their disease. This study highlights the performance of CEUS, its bowel indications, and contributions to patient management.
Sonographic evaluation of the bowel begins with identification of abnormal loops and determination of disease extent and location. US features of active disease include bowel wall thickening (> 3 mm for small bowel and > 5 mm for colon), hyperemia detected with CDI , the presence and amount of inflammatory fat and lymphadenopathy . These parameters allow for the selection of the most abnormal segment that can be studied with CEUS. Two important considerations when selecting the bowel segment for evaluation with CEUS include a well-visualized loop of bowel within the field of view with minimal or no peristalsis and bowel wall thickness of > 4 mm. This will ensure the best technical acquisition, especially for quantification. In our experience, loops in the lower quadrants, away from the influence of respiratory excursion, are optimal. In the majority of the cases, this is possible, as IBD most often affects the terminal ileum and the cecum. If an abnormal loop is identified with significant peristalsis, 20 mg IV of hyoscine butylbromide (Buscopan) over 1 min or glucagon 1 mg IV is used to minimize the bowel activity, if there are no contraindications. In our experience, antimotility medications are required in less than 10% of the cases of bowel CEUS.
Microbubble contrast agents
CEUS is performed on a fasting patient, using a microbubble contrast agent that enhances the ultrasound signals and allows for real-time evaluation of the vascularity . In Canada, our experience has been with perflutren microspheres, marketed as Definity (Lantheus Medical Imaging, Billerica, MA) . Sulfur hexafluoride, marketed as Sonovue (Bracco, Italy) in Canada, Europe, and Asia and Lumason in USA, is a similar agent with equivalent performance. These contrast-enhancing agents are gas-filled microbubbles with a phospholipid shell and are administered to the patient as a bolus intravenous injection [18, 21]. Microbubbles remain within the capillaries throughout the examination and they oscillate in the bloodstream in response to the application of an ultrasound field, producing non-linear harmonic frequencies that are detected at CEUS . Our standard volume of contrast agent for a bowel quantification study is generally twice the standard dose for liver mass evaluation: with perflutren lipid microspheres (Definity, Lantheus Medical Imaging) 0.4 ml, and with sulfur hexafluoride (Lumason, Bracco Diagnostics Inc) 4.8 ml, both followed by a 5 ml saline flush.
Machines and probes
The selected bowel is imaged with a high-resolution probe, in the frequency range of 5–9 MHz, using contrast-specific imaging techniques that currently are available on most high-end ultrasound systems. We choose the frequency optimal for the bowel evaluation which on our equipment is a C9-2 (EPIQ, Philips Bothell, WA) with a lower frequency reserved for occasional very large patients with deep bowel. Endovaginal probes with contrast capability also work exceptionally well to study deep ileal loops, in particular. Linear probes and high-resolution convex probes are also highly successful for evaluation of the perineum and anal canal.
Contrast imagining technique parameters include a low mechanical index and contrast-specific subtraction, whereby background tissue echoes are removed from the image so that a microbubble-only image is created.
Standard CEUS settings are contrast gain of 50–60%, mechanical index of 0.05, dynamic range of 40 dB, and focal zone set at maximal depth. We maintain the same parameters between examinations for standardization of the procedure. Obese patients and deeper bowel segments will reduce visualization and signal intensity; therefore, grayscale optimization is an important factor when performing bowel studies.
Although most US systems do allow for CEUS of the bowel and also generation of time–intensity quantification curves (TIC), there is considerable variability in the output of the machines which hampers the progress of this exciting technique. Additionally, many workstations, for quantification of blood flow, are machine/vendor specific which is additionally limiting. In our institution, we perform all of our quantifications with Q-Station (Philips Healthcare Ultrasound, Bothell WA). However, a more versatile system is VueBox (Bracco, Geneva, Switzerland) which is able to analyze data for quantification from all US systems following entry of 2D DICOM datasets provided by the vendors to Bracco.
Patients generally lie comfortably in a supine position. Quiet respiration is encouraged. To perform CEUS, the transducer is placed at the region of interest (ROI) selected on the initial grayscale assessment. The abnormal bowel segment is evaluated in a sagittal orientation to minimize out-of-plane effects of respiratory motion and to facilitate generation of quality TIC allowing for quantification analysis. After contrast is injected through the patient’s IV, a continuous acquisition is initiated, even before the arrival of the first bubble in the field of view, and lasting for 2 min with no motion of the transducer. Most ultrasound equipment will allow for initial evaluation of the quantification curves at the bedside to assess technical quality of the time–intensity curve and to obtain preliminary results. If CEUS fails, or is technically inadequate, a second contrast injection may be performed, after a several minute delay.
With experience, observation of the wash-in and decline of contrast agent in the bowel wall may be interpreted as reflective of mild disease with low peak and rapid decline and of more severe disease with a higher peak intensity and longer duration of enhancement.
In cases where the abnormal loop of bowel is deep within the pelvis, endovaginal B Mode and CEUS can be performed (Fig. 2). This excellent technique allows for close evaluation of the bowel with high-resolution US probes with great definition of wall abnormalities, in addition to superb capability to show blood flow and complications (Supplementary Videos 2 and 3). CEUS can also be performed using the endovaginal approach with creation of quantification curves (Fig. 2F).
An advantage of CEUS is the generation of time–intensity curves as an objective parameter of bowel enhancement. The recorded TICs can be analyzed using built in software on the ultrasound machine or using remote workstations. The raw native data from the 2-min Cine-clip stored in the US system are log compressed and exported in DICOM format to a PACS workstation or other analysis system, where the data are re-linearized. From these data, the linear TICs with appropriate curve fitting are generated allowing for measurement of blood flow parameters within the bowel wall.
Our software analysis system generates a printout for every patient including all of the parameters listed above, with the peak enhancement in dB and all other parameters generated from the curve of the log-normal linear data. To this date, we predominantly utilize the peak enhancement in dB, the AUC, measured in arbitrary intensity units, and the time to peak, in seconds for establishing an initial baseline activity assessment and to show changes over time with treatment or with natural disease progression (Fig. 4C, D). Subjective and objective observations of the TICs show that with severe disease, the PE is high and the decline may be delayed and at a higher enhancement level (yellow curve, Fig. 5B). On the other hand, with mild disease the PE enhancement is low and the decline is rapid and more closely reaches the baseline (red curve, Fig. 5B). These same assessments are more difficult to recognize when looking at the linear curves (Fig. 5A).
In centers in Europe, CEUS quantification analysis is often expressed as a percentage change of peak enhancement and of the AUC before and after treatment [21, 27, 28, 29]. In the study by Quaia , two ROIs are drawn, one in the thickest part of the anterior wall or covering the entire bowel wall in cases when the lumen was not visible and the second as an internal reference at the adjacent mesentery. TICs are also fitted with a non-linear least-squares regression method to a proprietary log-normal model with assessment of multiple curve parameters [30, 31]. These studies only compare exams between the same patient over time.
We prefer, instead, that this robust technique allows for integration of CEUS parameters with other established subjective and objective measures of disease activity, especially wall thickness and signal on color Doppler imaging,  to allow for categorization of disease between large numbers of patients and for more easily applied determinations of disease activity . In addition, it is invaluable for follow-up of patients over time.
Today, there is considerable variation in the output of US equipment for quantification techniques. This inconsistency in display makes acceptance of this technique for routine clinical applications a challenge and it is hoped that standardization of methods, displays, and reporting will occur in the near future as it has for other imaging techniques over time.
Indications for CEUS of the bowel
Determination of disease activity is most important when evaluating bowel inflammation. This is essential at the time of new diagnosis, during surveillance, to monitor treatment response and for the total assessment of symptomatic patients.
USGA with integration of CEUS
Performance of Ultrasound Global Assessment
Ultrasound features of activity
Wall thickness (mm)
Color Doppler imaging (CDI)
Small regions of color
No vessel structure
Medium vessel length
± Mesenteric vessels
Perienteric region resembles normal mesenteric fat
LESS AREA than the bowel on axial view
EQUAL AREA to the bowel on axial view
GREATER AREA than bowel on axial view
With integration of contrast-enhanced ultrasound (CEUS)—peak enhancement
CEUS PE (dB)
> 23 dB
Differentiation of strictures in IBD
Ultrasound is long recognized as a very reliable technique for the detection of strictures and associated incomplete mechanical bowel obstruction. This dynamic real-time technique shows dilated prestenotic segments and also evidence of dysfunctional peristalsis. Differentiation of strictures poses a frequent dilemma for imagers. This can be easily resolved by the addition of subjective and objective evaluation of the bowel blood flow with CEUS by showing the contribution of inflammation to the stricture and may be aided further by stiffness determination with elastography. Strictures in IBD may be inflammatory or chronic in nature. Differentiation of these two broad categories is recognized as a major role for imaging techniques as management differs. Several investigators have addressed the role of CEUS [40, 41, 42] and also elastography to characterize these strictures with ultrasound [42, 43]. Our own study shows that, in patients with chronic stenotic disease, smooth muscle hyperplasia/hypertrophy may contribute more to stricture than fibrosis  similar that to prior study by Baumgart . Additionally, we show an inverse relationship between velocity measurements on shear wave elastography and peak enhancement on CEUS. . Quaiai et al. show differentiation of inflammatory vs fibrotic strictures in which determination of active inflammation would favor the role of medical therapy .
Monitoring response to therapy
Medical therapy for patients with inflammatory bowel disease has evolved from the treatment of patient’s symptoms and complications to active efforts to modify the natural course of the disease by achieving mucosal healing as shown at endoscopy. Today, the use of long-term biologic therapies has changed the imaging management of this patient population with recognition that interval surveillance is a requisite component of treatment management. Additionally, medical therapy with steroids, immune modulators, and biologics all necessitate imaging surveillance to assess for treatment response and detection of complications in these immunosuppressed patients. Various publications have shown that the use of CEUS with TIC analysis can differentiate pharmacologic therapy response and identify non-responders [29, 30]. This distinction is very important for patient outcome and prognosis. Early recognition of inadequate treatment response would alleviate a long, expensive, and ineffective treatment .
Therapy response can be categorized as showing complete positive response, no response, or various grades of partial response. We do this grading by evaluating all parameters shown on grayscale and also on CEUS. While a complete positive response may lead to virtual resolution of all observations, more often a partial response may only show reduction of the CEUS parameters with the grayscale and CDI parameters continuing to suggest active disease. CEUS with grayscale evaluation may also show complete lack of response suggesting the necessity of dose escalation or change of therapeutic regime. Surveillance scans are performed of all patients on biologic therapy as inflammatory parameters are recognized as unreliable determinants of disease.
Additional uses of CEUS in bowel disease
In IBD and other bowel conditions, there is a potential for development of inflammatory masses representing fluid containing abscesses or phlegmons, where there may be severe inflammation but no actual drainable pus. Differentiation of these masses on grayscale US is often challenging as there is a strong tendency for overlap in their US imaging appearance with all frequently showing as a hypoechoic mass. This distinction is of extreme clinical significance, as management, prognosis, and therapy differ .
The study of inflammatory masses with US may be influenced by probe selection and placement. It includes the advantage of endovaginal scan in women, where the frequently involved pouch of Douglas is ideally evaluated and also the transperineal placement, in men and women, for confirmation of perianal abscess (Fig. 3). Inflammatory polyps may be suspected and confirmed as intraluminal vascular masses (Fig. 8A and Supplementary Video 9).
Appendicitis and diverticulitis
Acute inflammatory conditions of the bowel include especially appendicitis and diverticulitis. At presentation, patients may have bowel perforation and/or an inflammatory mass, similar to those already shown with IBD. As previously described, these inflammatory masses can be further characterized with CEUS to differentiate phlegmon and abscess, as their clinical management would be different (Fig. 7).
Furthermore, CEUS may be a helpful adjuvant in early detection of wall ischemia, as a sign of gangrenous appendicitis that can be a precursor of perforation [37, 48]. In a study including 50 patients with suspected appendicitis, CEUS was 100% accurate in the identification of suppurative and gangrenous appendicitis when compare to surgical and histological findings .
Chronic diverticular disease may occasionally show colonic wall thickening and pseudomasses of uncertain etiology. This persistent hypoechoic wall thickening, in the absence of acute inflammatory changes, is most often related to familiar muscular hypertrophy.
This rare self-limiting inflammatory/ischemic process of the appendix epiploica of the colon may present as a hypo- and hyperechoic mass-like area next to the colonic wall at the site of patient’s pain that will enhance on CEUS as an inflammatory mass with a central area of non-enhancement that represents the central thrombosed pedicle, as occasionally seen on CT as the hyperdense central dot sign .
Colitis and graft versus host disease (GVHD)
CEUS is only helpful for identification and grading of inflammation. However, it is not useful for differentiation of infectious colitis. CEUS has being described to be used only in a few instances where detection of wall necrosis or abscess may be a feature of condition, such as in cases of neutropenic enterocolitis [48, 51].
A few studies with a small number of patients also hypothesized that CEUS could detect microcirculatory changes of the bowel wall during evaluation of GVHD and to monitor therapy in this condition [48, 52].
Bowel ischemia can be present due to bowel strangulation, thrombosis of the SMA, or non-occlusive mesenteric ischemia in patients with bowel obstruction. Patients with ischemia may have thin bowel walls as a result of loss of bowel wall tissue, vascularity, and muscular tone .
Studies have shown that lack of or decreased CEUS enhancement of the bowel wall is a hallmark for bowel ischemia with sensitivity of 85–94% and specificity of 100% . In the case of bowel obstruction, this is seen most commonly in the least peristaltic segment and/or in the most dilated bowel segment .
In addition, CEUS has been used in other centers for adequate visualization of the visceral arteries. A European study combined CEUS with color and spectral Doppler allowing for an unequivocal diagnosis of visceral artery stenosis in patients with abdominal angina .
As in other contrast imaging modalities, CEUS can delineate the tumor extent and vascularity very well. Some studies suggest that dynamic contrast-enhanced ultrasound with vascular recognition imaging software enables detection of micro-vessels and quantification of tumor perfusion. This has been used for assessment of treatment response and was correlated with survival .
CEUS can easily detect viable enhancing tumor versus areas of necrosis to guide target biopsy sampling and to minimize inadequate or insufficient sampling errors. This is particularly important in gastrointestinal stromal tumors (GIST) which can present as small or large masses within the peritoneal cavity, with or without an obvious attachment to a loop of bowel. They frequently show large areas of central necrosis or cystic degeneration, which is frequently suggestive of their diagnosis (Fig. 8F and Supplementary Video 14). On CEUS, GIST tumors show as a hypervascular mass in the arterial phase followed by slow wash-out during the portal venous phase . In addition, in a small study of 24 patients with GIST, CEUS allowed for early prediction of tumor response to Imatinib treatment .
As compared with inflammation of the bowel which most often will involve a long segment, generally showing a stratified wall layering, most tumors show instead as a focal black mass, generally with complete wall layer destruction. Focal round masses of small and medium size identified incidentally during scans performed for IBD surveillance are often carcinoid (Fig. 8B, Supplementary Video 10 and 8E, Supplementary Video 13) or neuroendocrine tumors. They are highly vascular on CEUS and their wash-out correlates with their malignant potential .
Lymphoma and adenocarcinoma
Lymphoma may show additionally an aneurysmal pattern of luminal expansion and lymph node involvement. (Figure 8C, Supplementary Video 11). Perienteric fat infiltration may be associated with all tumors.
Adenocarcinoma is seen most often in the large bowel although small bowel tumors are more prevalent in the population with IBD as compared with the general population (Fig. 8D, Supplementary Video 12).
Conclusions—role of CEUS
CEUS may be utilized in evaluation of the bowel providing information about mural and mesenteric blood flow in a wide variety of situations. Similar to the use of intravascular contrast agents for CT and MR enterography, the addition of contrast agents to US will provide valuable information wherever blood flow knowledge would be helpful. However, it is in the evaluation of the population with IBD where the addition of CEUS has had its greatest clinical impact, substantially improving the role of ultrasound in the evaluation of the bowel. Although CDI is invaluable in bowel assessments, it has shortcomings which are easily overcome with CEUS. In addition, CEUS provides both subjective and objective quantification of mural blood flow. This is particularly important in the young population with IBD that requires frequent imaging surveillance and follow-up throughout the course of this chronic disease. Ultrasound and CEUS provide a non-invasive and accurate assessment of the classic features of CD and are highly sensitive for the detection and diagnosis of complication. In the future, CEUS of the bowel should be regarded as an essential component of standard care for imaging of the bowel in IBD.
Compliance with ethical standards
Conflict of interest
Alexandra Medellin received equipment support from Siemens Healthineers (unrelated to this publication). Christina Merrill declares no conflict of interest. Stephanie R Wilson received equipment support from Philips Healthcare Ultrasound (related to this publication), equipment support from Siemens Healthineers and Samsung (unrelated to this publication), speaker honorarium from GE and Samsung within the last 3 years, and contrast agent support (unrelated to this publication) from Lantheus Medical Imaging.
As this is a review article rather than a study, we do not have IRB approval. Nor do patients provide signed informed consent.
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