Multiparametric ultrasound in the diagnosis and monitoring of ischemic colitis: description of a case of ischemic colitis of the right colon and revision of the literature

Abstract

The aim of this paper is to describe the usefulness of multiparametric US in the diagnosis and subsequent follow-up of a case of right-side ischemic colitis and to present a review of the data reported in the literature. Ischemic colitis is frequently diagnosed in the field of gastroenterology. Diagnosis is usually based on the outcome of endoscopy and histological examination, and in case of right-side ischemic colitis also on the results of contrast-enhanced CT. In the described case, multiparametric US indicated the diagnosis including a prognostic judgment, and during follow-up US-monitored patency of the stents positioned under angiographic guidance. One of the available US techniques, CEUS, seems to have a special role in the detection of residual vascularization of the gastrointestinal tract affected by ischemia. However, before introducing this method into daily clinical practice, further studies are required to confirm its diagnostic accuracy.

Introduction

Ischemic colitis is a common vascular disorder in the elderly. It is probably linked to damage to the bowel wall due to hypoperfusion/reperfusion caused by a combination of factors (sudden systemic hypotension, anatomic or functional changes in the splanchnic vessels or in the microcirculation of the colon wall) [1].

Ischemic colitis mainly affects patients who are debilitated, and it is generally associated with diseases of the cardiovascular system and/or renal disorders, or with the use of multiple medications. In younger subjects, it is usually linked to hemocoagulative disorders or inflammatory vasculopathy [1].

In the last 10 years, ischemic colitis affecting the right side of the colon has been associated with a worse prognosis in terms of morbidity and mortality than ischemic colitis of the left side. This is due to a more frequent association with cardiovascular pathologies, atherosclerosis of the mesenteric vessels and to a certain risk of subsequent acute mesenteric insufficiency in some patients [2].

The aim of this paper is to describe the usefulness of multiparametric ultrasound (US) in the diagnosis and subsequent follow-up of a case of right-side ischemic colitis, to evaluate the addition of more recent diagnostic methods, such as strain elastography (SE) and contrast-enhanced US (CEUS) to obtain a more accurate staging of this disease and to present a short review of the literature.

Case report

A 61-year-old woman, former smoker, suffering from chronic autoimmune thyroiditis, arterial hypertension and recent myocardial infarction as well as occlusion of the right iliac artery due to atheromatous plaque, came to the emergency room complaining of abdominal pain particularly in the right hypochondrium and subsequent gastrointestinal bleeding (dark red blood). She reported a change in the bowel movement pattern starting 2 months before with postprandial diarrhea but no abdominal pain.

Upon admission to the emergency room, the patient’s clinical condition was relatively good with normal blood pressure and heart rate and basic laboratory values were normal with the exception of moderate leukocytosis. The patient was referred to our gastroenterological clinic because of hematochezia and underwent physical examination as well as abdominal US.

US was performed using a scanner (Mylab Twice, Esaote, Italy) with appropriate convex and linear probes (CA541 1–8 MHz, LA332 3-11 MHhz) and software dedicated to SE and CEUS.

SE provides an evaluation of the “relative” elastic properties of the tissues in a region of interest (ROI). Our scanner shows the elasticity values in 100 color shades from blue ‘‘maximum stiffness’’ to red “maximum elasticity”. In diseases of the gastrointestinal tract, SE usually documents and quantifies the loss of physiological elasticity of the bowel walls [3].

CEUS was performed on the affected colon wall using a contrast agent based on sulfur hexafluoride microbubbles (SonoVue, Bracco, Italy) administered as an intravenous bolus of 2.4 ml. The examination was recorded for further processing using the software available in our institution (VueBox v7.0, Bracco SA, Geneva, Switzerland) which allows calculation of time/intensity curves (TIC) and some parameters related to the perfusion of the studied target. The use of this software is described in a previous paper [4]. CEUS examination of the celiac tripod and the inferior mesenteric artery was performed by administering a smaller bolus (1.2 ml) of SonoVue, and the obtained clip was recorded for subsequent computer evaluation.

B-mode US showed symmetrical pathological thickening (8–10 mm) of the cecal wall and ascending colon with loss of physiological echostratification, but no changes in the echogenicity of the paracolic gutter tissue and no peritoneal fluid (Fig. 1a). The walls of the transverse, descendant and sigmoid colon presented normal thickness with preserved echostratification.

Fig. 1.

Multiparametric US of the ascending colon. a Color Doppler US, longitudinal scan, shows wall thickening with poor vascular signals. b The same portion of the colon: PW Doppler US evidences continuous flow. c Color and PW Doppler US focused on the celiac trunk shows focal aliasing (arrow) near the origin of the vessel arising from the aorta and an abnormal velocitogram with systolic peak velocity > 454 cm/s. d Color Doppler US shows occlusion of the superior mesenteric artery (arrowhead) where it arises from the abdominal aorta and revascularization in the adjacent portion (arrow)

Color Doppler US of the thickened intestinal walls yielded only weak vascular wall signals, and pulsed wave (PW) Doppler US showed mainly velocitograms with low systolic peaks or continuous flow (Fig. 1b). Color and PW Doppler US of the celiac and superior mesenteric arteries furthermore showed stenosis of the celiac trunk and absence of blood flow at the origin of the superior mesenteric artery with retrograde revascularization of the artery about 3 cm from the ostium (Fig. 1c, d).

SE focused on the thickened ascending colon walls showed a blue layer in the mucous tunic and adjacent submucosa (Fig. 2a) interpreted as loss of elasticity due to hemorrhage or interstitial edema. It is important to note that the normal bowel wall is mainly green on the SE image with shades of blue in the mucous tunic and more clearly defined blue lines in the muscular tunic [3–5].

Fig. 2.

SE and CEUS longitudinal scan at the level of the ascending colon and the ileocecal valve. a SE shows partially preserved color stratification of the colon wall with reduced elasticity of the mucous tunic (blue ***) compared to the muscular and serous tunics (green) and adjacent pericolic tissues (arrowhead: ileocecal valve). b CEUS, the same scanning session as a), shows enhancement of the pathologically thickened colon wall with slight hypoperfusion of the mucosal tunic (arrow). c Elaboration of enhancement data obtained in the ROI drawn on the colon wall, TIC curve and semiquantitative measures: PE maximum enhancement value, wash-in AUC enhancement values under the wash-in curve (red area). d TIC curve in a case of left ischemic colitis (confirmed at endoscopy and histological examination) without disease affecting the visceral arteries.e Distribution of wash-in AUC (parameter related to the vascular network in the ROI) is inhomogeneous with low values in some portions of the ROI (arrowheads). d Distribution of RT (parameter related to blood flow velocity in the ROI) is inhomogeneous and prolonged in the portions of the ROI presenting low wash-in AUC values (arrowheads)

CEUS showed perfusion of the examined portions of the bowel wall, but also a certain perfusion inhomogeneity with possible hypoperfused areas of the mucous tunic (arrow, Fig. 2b).

Processing of CEUS enhancement data using quantification software permitted calculation of a TIC curve and parametric images related to the enhancement pattern obtained in the ROI drawn on the affected colon wall. The TIC curve was characterized by a slower wash-in and wash-out phase as compared to other cases of ischemic colitis that have previously come to our observation (Fig. 2c, d). The parametric images of the affected bowel wall were characterized by an uneven distribution of the values of the chosen parameters suggesting a rather inhomogeneous vascular architecture with areas of mucosal hypoperfusion (Fig. 2e, f).

Endoscopy performed a few days after admission to hospital revealed superficial ulcers and erosions alternating with areas of edematous and hyperemic mucosa. Histology confirmed ischemic colitis.

Contrast-enhanced CT confirmed stenosis of the celiac trunk, stenosis of the ostium of the inferior mesenteric artery and occlusion at the origin of the superior mesenteric artery. Angiography was subsequently performed with correction of the two stenoses.

Clinical evolution was favorable and the patient’s condition is good 12 months after this acute episode. B-mode US follow-up (about 2, 8 and 12 months after discharge) showed gradually reduced thickening of the colon walls affected by the ischemic episode and progressively restored echostratification of the ascending colon wall (Fig. 3a, b).

Fig. 3.

Multiparametric US follow-up: a, b B-mode US longitudinal scans of the ascending colon 2 and 12 months after discharge evidence reduced (2 months) and normal (12 months) colon wall thickness with restored echostratification. c CEUS longitudinal scan of the ascending colon 12 months after discharge shows normal wall thickness and wall enhancement similar to that of the adjacent paracolic gutter. d TIC representing colon wall enhancement is characterized by a slow wash-in phase suggestive of persistent changes in the splanchnic hemodynamics despite positioning of the two stents. e, f CEUS follow-up of the stent positioned at the origin of the celiac trunk shows complete patency of the stent (e 2 months after discharge) and early stenosis (f 8 months after discharge)

CEUS of the ascending colon wall was repeated after 12 months. The examination was difficult due to thinness of the colon wall; enhancement was slightly inhomogeneous and the intensity was similar to that of the adjacent paracolic gutters (Fig. 3d). Color Doppler and CEUS follow-up of the positioned stents (2, 8 and 12 months after discharge) evidenced early stenosis of the stent in the celiac trunk (8 months after discharge, Fig. 3f) and persistent patency of the stent positioned in the inferior mesenteric artery. After regression of the acute phase, SE follow-up was not possible due to bowel contents in the ascending colon.

Discussion

Ischemic colitis is frequently diagnosed in the field of gastroenterology, particularly in patients with acute onset of abdominal pain, diarrhea and hematochezia. If the ascending colon is affected by ischemia, occlusive disease of the splanchnic vessels should be suspected.

According to the data reported in the literature, diagnosis is based on the outcome of endoscopy, histological examination and contrast-enhanced CT aimed at identifying the affected portion of the colon and possible complications outside the colon as well as assessing the integrity of the mesenteric vessels [6]. Angiographic procedures and surgery are performed in more severe cases which do not resolve spontaneously or after medical therapy.

The purpose of this case report is to present the usefulness of recently developed US methods performed in a patient with ischemic colitis and to present a review of the data reported in the literature. Reports on the use of US in this disease are not frequent in the literature; the method is considered operator dependent and hindered by the presence of intestinal gas and/or by the physical constitution of the patient, but also because color Doppler US is reliable only in the study of the proximal portion of the mesenteric vessels.

On the basis of studies reported in the literature, US findings in this disease using B-mode, color Doppler and duplex US can be summarized as follows (Table 1).

Table 1.

US findings in ischemic colitis reported in the literature

Authors	US method	US findings in ischemic colitis
Cheung et al. [7] Ripolles et al. [8] Danse et al. [9, 12] Pastor-Juan et al. [13]	B-mode	Thickening of the colon wall, segment > 10 cm or diffuse Moderate/severe wall thickening > 5 mm Loss of wall echostratification Changes in the pericolic fat Presence of intraperitoneal fluid
Ripolles et al. [8] Danse et al. [9, 12] Teefey et al. [10]	Color Doppler Duplex	Absent or barely visible vascular wall signals Resistive Index of vascular wall signals > 0.60 Stenosis of at least two splanchnic arterial vessels

B-mode US has a high sensitivity in the diagnosis of this disease (> 90% [7, 8]), but specificity is low as other mainly inflammatory diseases may yield similar findings [9, 10]. Absent or barely visible color Doppler signals from the pathologically thickened colon walls are highly specific signs of ischemic colitis, but this finding is encountered only in 20–50% of cases [8–10]. However, if color Doppler US yields vascular wall signals, resistance index > 0.60 can discriminate between ischemic and inflammatory disease [10]. It should be pointed out that the combination of acute abdominal pain and hematochezia associated with US finding of a long colon segment with thickened walls is highly predictive of ischemic colitis in elderly patients (PPV > 87%) [11].

With regard to the possibility of a prognostic judgment, some studies suggested a correlation between loss of bowel wall echostratification [7] or absence of vascular bowel wall signals [12] and more severe ischemic episodes. These results were not confirmed in a more recent study in which only pericolic adipose tissue alteration and/or pancolitis showed a statistically significant correlation with a less favorable prognosis [13].

The described case is peculiar as the severe condition of the splanchnic vessels was asymptomatic over a long period of time until the onset of abdominal pain associated with hematochezia.

In this clinical context, B-mode US detection of a long colon segment with moderate to severe wall thickening and loss of wall echostratification was predictive of an ischemic injury.

Color Doppler US confirmed the diagnosis by showing barely visible vascular wall signals and by detecting changes affecting the origin of the splanchnic vessels.

There are no data in the literature regarding the use of SE in ischemic colitis. The studies involving SE mainly deal with Crohn’s disease and the possibility of distinguishing fibrotic scarring from inflammation. In our initial experience, SE has not provided a differential diagnosis between the various diseases of the colon [14]. However, in ischemic colitis minor changes in the elasticity of the affected wall usually correspond to clinical and endoscopic findings of low severity [14].

In the present case, preserved color stratification of the intestinal wall and reduced elasticity (hemorrhage/interstitial edema) limited to the mucous tunic and to the superficial layers of the submucosa seemed to suggest ischemic injury affecting only these tunics.

CEUS is a US method known and used in Europe, Asia and North America. The most widespread areas of application are characterization of benign and malignant primary lesions of the liver and detection of secondary lesions of the liver. The diagnostic accuracy of the method is clearly superior to that of B-mode US and color Doppler US and similar to that of contrast-enhanced CT and contrast-enhanced MRI. A recent review [15] and the SIUMB Guidelines [16] suggest the correct method of execution and clinical indications.

Extrahepatic CEUS (pancreas, spleen, kidneys, prostate, bowels and aorta) are more recent applications. Some indications for CEUS are now well established, while others [17] require further studies before being introduced into clinical practice [18]. With regard to the use of CEUS in diseases of the gastrointestinal tract, current indications are limited to Crohn’s disease [18] (assessment of inflammatory wall activity, differential diagnosis between inflammatory and fibrotic stenosis, monitoring of response to therapy and detection of possible abscesses).

To our knowledge, no studies addressing the use of CEUS in ischemic colitis have been reported in the literature. Two studies using first-generation US contrast agent (Levovist) in patients with acute mesenteric ischemia showed weak or absent enhancement of the ischemic bowel walls compared to those receiving blood supply [19, 20]. CEUS using a second-generation contrast agent (SonoVue) showed both vascular occlusion and concomitant acute bowel ischemia in a patient with embolism of the superior mesenteric artery [21].

In the described case, CEUS proved useful suggesting a better prognosis by showing adequate perfusion of the affected segment of the colon, whereas B-mode US showed wall thickening with loss of echostratification and color Doppler US yielded only scarce and weak vascular signals.

Processing of CEUS enhancement data using quantification software permitted calculation of the time/intensity curve (suggestive of changes in the splanchnic hemodynamics due to a very slow wash-in phase) and parametric images of the affected colon wall (suggestive of relative hypoperfusion of some areas of the mucous and submucosal tunics).

Later, CEUS proved useful for monitoring the patency of the stents positioned under angiographic guidance and in the evaluation of the colon walls, by that time normal at B-mode US.

Conclusions

We describe a case of right-side ischemic colitis in which we used the available US methods (B-mode US, color Doppler US, SE and CEUS) to collect and compare the information required for the diagnosis and subsequent monitoring of the disease.

In accordance with the data reported in the literature, we believe that B-mode US and color Doppler US carried out in the initial workup of patients with abdominal pain and hematochezia may in most cases suggest a diagnosis of ischemic colitis by evidencing a long segment of the colon with thickened walls yielding weak vascular signals.

In this case, the role of SE was limited to the acute phase of the disease.

In our opinion, CEUS can in selected cases play an additional role by depicting bowel wall microcirculation and thus improve the accuracy of prognostic estimates.

Evaluation of the splanchnic vessels and monitoring of the patency of stents positioned under angiographic guidance are usually possible using color Doppler US. CEUS is a relatively invasive method requiring venous access and it is expensive, but it can be useful in selected cases to increase diagnostic confidence.

Finally, elaboration of enhancement values using dedicated software to obtain TIC curves and parametric images (wash-in AUC and RT) of the damaged wall may suggest a differential diagnosis between ischemic colitis and various inflammatory colon diseases, but targeted studies are required to confirm this hypothesis.

Funding

This study was not funded by third parties.

Compliance with ethical standards

Conflict of interest

Andrea Giannetti declares personal fees from Bracco Suisse S. A., outside the submitted work. Marco Matergi, Marco Biscontri, Lucia Falconi, Francesco Tedone, Valeria Ussia, Luca Giovannelli, Luca Franci and Massimo Pieraccini declare that they have no conflict of interest related to this study.

Informed consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000. The patient provided written informed consent to the publication of information that could potentially lead to her identification.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.