Gastrointestinal Imaging Review

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1 Gastrointestinal Imaging Review Huprich et al. CT Enterography of Small-Bowel Vascular Lesions Gastrointestinal Imaging Review FOCUS ON: James E. Huprich 1 John M. Barlow 1 Stephanie L. Hansel 2 Jeffrey A. Alexander 2 Jeff L. Fidler 1 Huprich JE, Barlow JM, Hansel SL, Alexander JA, Fidler JL Keywords: angioectasia, CT, CT enterography, obscure gastrointestinal bleeding, small-bowel vascular lesions DOI: /AJR Received December 5, 2012; accepted after revision January 29, J. E. Huprich and J. L. Fidler have received research support from Bracco Diagnostics. S. L. Hansel has received educational support from Given Imaging. 1 Department of Radiology, Mayo Clinic, 200 First St SW, Rochester, MN Address correspondence to J. E. Huprich (huprich@mayo.edu). 2 Department or Gastroenterology and Hepatology, Mayo Clinic, Rochester, MN. AJR 2013; 201: X/13/ American Roentgen Ray Society Multiphase CT Enterography Evaluation of Small-Bowel Vascular Lesions OBJECTIVE. By use of multiphase CT enterography (CTE), small-bowel vascular lesions associated with gastrointestinal bleeding can be classified into three categories angioectasias, arterial lesions, and venous abnormalities on the basis of common morphology and enhancement patterns. This article will review the unique patterns of enhancement and lesion morphology seen on multiphase CTE and how those findings enable detection and characterization of specific lesions in many cases. CONCLUSION. Because of the high prevalence in nonbleeding patients and frequent multiplicity of angioectasias, determining the clinical benefit from their detection by multiphase CTE and endoscopy is problematic. Although arterial lesions are less commonly encountered clinically, their detection is critically important because of a high risk of life-threatening bleeding. Along with wireless capsule endoscopy and balloon-assisted endoscopy, multiphase CTE is a useful tool for the evaluation of patients with obscure gastrointestinal bleeding due to small-bowel vascular lesions. V ascular lesions of the small-bowel represent a pathologically diverse group of abnormalities that are reported to account for up to 40% of cases of obscure gastrointestinal bleeding (defined as persistent or recurrent gastrointestinal bleeding in the face of normal upper endoscopy and colonoscopy) [1]. Until recently, most small-bowel abnormalities could only be detected by angiographic or surgical techniques. Wireless capsule endoscopy and balloon-assisted endoscopy have revolutionized the evaluation of small-bowel bleeding, actually allowing direct visualization of the small-bowel mucosal surface. However, each of these techniques has some disadvantages. Although relatively noninvasive, capsule endoscopy can be associated with a 30% rate of false-positive findings [2], up to a 20% rate of incomplete small-bowel evaluation [3], and a small risk of capsule retention, sometimes necessitating endoscopic or surgical removal. Capsule endoscopy also may fail to detect small-bowel masses particularly malignancies that arise in the submucosa, which may cause little mucosal disruption [4, 5]. Balloon-assisted endoscopy allows the diagnosis and treatment of many small-bowel abnormalities but requires a high level of technical expertise; is time-consuming; and risks bowel injury, including perforation. The recent development of multiphase CT enterography (CTE) has proven useful in the evaluation of obscure gastrointestinal bleeding [6, 7].The purpose of this article is to describe multiphase CTE technique and findings in small-bowel vascular lesions associated with obscure gastrointestinal bleeding, to suggest a classification of these lesions on the basis of multiphase CTE findings, and to discuss the role of multiphase CTE in the diagnosis and management of these vascular lesions in conjunction with balloon-assisted endoscopy and capsule endoscopy. Multiphase CT Enterography Technique Patients referred for multiphase CTE should show evidence of obscure gastrointestinal bleeding, defined as persistent or recurrent gastrointestinal bleeding in the face of normal upper endoscopy and colonoscopy. Obscure gastrointestinal bleeding may be manifested as iron deficiency anemia or positive fecal occult blood test (occult subtype) or as hematochezia or melena (overt subtype). Because of the high spatial and temporal resolution required, these examinations are best performed on a 64- or 128-MDCT system. Large volumes of neutral enteric AJR:201, July

2 Huprich et al. contrast material are needed to distend the bowel lumen in the setting of obscure gastrointestinal bleeding. Although a number of different methods may be used, our method [6] is for patients to ingest a total of 1350 ml of 0.1% weight/volume barium sulfate suspension (VoLumen, E-Z-EM) orally, divided into three 450 ml doses administered every 15 minutes beginning 60 minutes before scanning. An additional 500 ml of water is administered orally 15 minutes before scanning. A 4-hour fast precedes administration of the oral contrast material, and 150 ml of iohexol (Omnipaque 300, GE Healthcare) is power injected IV at a rate of 4 ml/s through an antecubital catheter. Scanning is performed from the diaphragm to the symphysis pubis during each of three phases: a bolus-triggered arterial phase; an enteric phase beginning 50 seconds after the beginning of injection, and a delayed phase 90 seconds after the beginning of contrast injection using a 64- or 128-MDCT system. Bolus triggering is performed by the CT technologist by placing a region of interest (ROI) cursor over the descending aorta 2 cm above the diaphragm. The ROI trigger threshold is set at 150 HU at 120 kvp, with scanning initiated 6 seconds after the threshold CT number is achieved. Patients are scanned at 120 kvp with a quality reference effective tube current exposure time product of mas. Detector collimation is set to the minimum slice width. For each phase of acquisition, axial images are reconstructed using a 2-mm slice width and 1-mm reconstruction interval. Coronal multiplanar images are reconstructed from the retroperitoneal border to the anterior abdominal wall at 2-mm slice width and 1-mm reconstruction interval. Interpretation of these studies can be challenging 2-mm slices in axial and coronal planes covering the entire abdomen and pelvis repeated for three phases can generate images per case. Added to this, the fact that lesions may consist of a tiny nidus of enhancement visible on only one of the three phases adds additional challenge. It is necessary to have a strategy for viewing these studies to maximize chances for successful interpretation. We read all our studies on a dual-monitor workstation. Our method of review consists of placing the enteric phase on the left monitor and the arterial and delayed images on the right one above the other. All images are synchronized so that identical anatomic locations are displayed for each phase while scrolling through the images. Viewing each phase simultaneously enables appreciation of the evolving nature of enhancing lesions. Once a suspicious area is found, the corresponding coregistered coronal images are examined to determine the approximate location and lesion shape. Maximum intensity projection may be useful for detecting feeding arteries and draining veins associated with some vascular lesions. Although this technique is specifically designed to detect small-bowel abnormalities responsible for bleeding, the entire gastrointestinal tract should be examined. We know from previous reports that endoscopy fails to detect endoscopically accessible lesions in the upper gastrointestinal tract in up to 26% of patients [8]. It is therefore important when interpreting multiphase CTE examinations not only to evaluate the small-bowel but also to carefully examine the upper gastrointestinal tract and colon. A poorly prepared colon, a primary submucosal location, or a location behind a fold may prevent detection of a lesion at colonoscopy that may be visible on multiphase CTE. Types of Vascular Lesions The terminology used in the literature to describe vascular lesions of the gastrointestinal tract is confusing, with different terms often used interchangeably. The classification of these lesions has not been standardized, and this deficiency has contributed to the confusion surrounding the understanding of these abnormalities. To clarify these issues, Yano et al. [9] proposed classification of small-bowel vascular lesions on the basis of endoscopic findings in 102 cases of TABLE 1: Endoscopic Classification of Small-Bowel Vascular Lesions [9] obscure gastrointestinal bleeding associated with vascular lesions. Their classification includes four basic categories (Table 1). Type 1 lesions correspond with the most common type of angioectasias observed endoscopically and represented 91% (93/102) of the abnormalities. Type 2 and 3 lesions are differentiated by their pulsatile character and consist of arterial lesions such as Dieulafoy lesions and arteriovenous malformations (AVMs). These arterial lesions made up 8% (8/102) of their cases. A single type 4 lesion was described as a vascular lesion with unusual morphology and is unclassifiable. Lesion morphology and enhancement pattern in small-bowel vascular lesions seen at multiphase CTE correlate well with the endoscopic classification of the study by Yano et al. [9]. On the basis of multiphase CTE findings, we propose a classification of vascular abnormalities that includes three types of lesions: angioectasias (type 1 lesions by Yano et al.), arterial lesions (type 2 and 3 lesions by Yano et al.), and venous lesions. Each type of lesion is distinguished by a common morphology and enhancement pattern (Fig. 1). The pathology, multiphase CTE appearance, and clinical significance of each type of lesion will be discussed in the following sections. In our practice, which consists principally of hemodynamically stable outpatients, active bleeding is relatively uncommon. When present, active bleeding is manifested as the progressive accumulation of intraluminal contrast material displayed over the three phases. The extravasated contrast material may pool on the dependent surface of the bowel or may be dispersed by peristalsis into a more irregular shape. Active bleeding should be suspected whenever one sees a contrast material collection that expands in size over subsequent phases (Fig. 2). Angioectasias Much of what we know about angioectasias (also known as angiodysplasias ) is based on findings at colonoscopy [10], although there is no evidence to suggest that small-bowel an- Lesion Category Endoscopic Description Pathologic Correlate Incidence (%) Types 1a and 1b Punctate (1a) or patchy (1b) erythema with or without oozing Angioectasia 91 Types 2a and 2b Punctate lesions with pulsatile bleeding (2a) or pulsatile red protrusion without Dieulafoy lesions 4 surrounding venous distention (2b) Type 3 Pulsatile red protrusion with surrounding venous dilatation Arteriovenous malformation 4 Type 4 Other lesions not classified into any other category All others 1 66 AJR:201, July 2013

3 CT Enterography of Small-Bowel Vascular Lesions Enhancement Arterial lesions Arterial Angioectasias Enteric Acquisition Phase gioectasias differ in any significant way from colonic lesions. Angioectasias are reported to be the most common cause of obscure gastrointestinal bleeding [1] and consist of thin tortuous veins that lack an internal elastic layer. Endoscopically, angioectasias consist of punctate or patchy areas of erythema, 2 10 mm in size (Fig. 3). They often have a classic arborizing pattern and may bleed easily on contact. The peak incidence of these lesions is in the 7th and 8th decades of life. Reports indicate that angioectasias are multiple in 40 75% of patients with gastrointestinal bleeding. Additionally, angioectasias are seen at colonoscopy in % of patients undergoing the procedure for a variety of indications [10]. Hemingway [11] detected colonic angioectasias by angiography in 3.6% of 166 patients evaluated for reasons other than bleeding. Small-bowel angioectasias are reported in up to 50% of patients undergoing capsule endoscopy studies for obscure gastrointestinal bleeding [3]. Venous lesions Delayed Fig. 1 Graph shows enhancement characteristics of smallbowel vascular lesions causing gastrointestinal bleeding. These reports suggest that many of the angioectasias detected by endoscopy or multiphase CTE are incidental and may not be associated with bleeding. These findings may help explain why bleeding commonly recurs after successful treatment of small-bowel and colonic angioectasias [12, 13]. The cause of angioectasias is uncertain. Boley et al. [14] suggested that colonic angioectasias are acquired and are the result of a degenerative process associated with aging. These authors suggested that colonic angioectasias are caused by chronic intermittent low-grade obstruction to venules, capillaries, and arteries of the mucosal vascular unit. Ultimately, precapillary sphincters lose their competency, producing small arteriovenous communications (Fig. 4). Boley et al. also suggested that these lesions are present with or without bleeding in a significant portion of the population more than 60 years old and are multiple more often than solitary. Although these observations pertain to colonic angioectasias, the similarity in endoscopic appearance, prevalence, and clinical behavior of small-bowel angioectasias compared with colonic angioectasias suggests a common cause. The appearance of angioectasias on multiphase CTE consists of focal punctate or discoid areas of enhancement less than 5 mm in size (Fig. 5) or bulbous swelling of the intramural vessels in the wall of the smallbowel, especially in the jejunum (Fig. 6A). The latter appearance is seen not only in patients with obscure gastrointestinal bleeding but also in nonbleeding patients more than 50 years old. Whether these bulbous lesions represent normal vessels or asymptomatic angioectasias is unknown. Indeed, photomicrographs of resected surgical specimens in patients with angioectasias in the study by Boley et al. [14] closely resembled multiphase CTE findings in some patients with endoscopically proven cases of angioectasias (Fig. 6B). Enhancement of angioectasias is brightest during the enteric phase and fades somewhat during the delayed phase. These lesions seldom enhance during the arterial phase, which distinguishes them from arterial lesions. Likewise, an enlarged feeding artery or early draining vein is usually not seen. Arterial Lesions Arterial lesions include Dieulafoy lesions, arteriovenous fistulas (AVFs), and AVMs. Because these lesions are exposed to high arterial pressure, there is a significant potential for life-threatening bleeding. A Fig. 2 Active bleeding in 82-year-old woman on warfarin therapy for aortic valve replacement who experienced melena and anemia with negative capsule endoscopy. (Reprinted with permission from [7]) A C, Axial arterial (A), enteric (B), and delayed (C) phase images from multiphase CT enterography show progressive accumulation of contrast material in dependent portion of small bowel (arrow) due to active bleeding from ileal ulcer, confirmed surgically. B C AJR:201, July

4 Huprich et al. Fig year old woman with angioectasia. Endoscopic image shows appearance of angioectasia (arrow) with 2 10 mm irregular patchy area of erythema. Dieulafoy lesions, also known as caliber persistent arteries, are relatively uncommon but can potentially cause life-threatening bleeding [15]. These lesions may cause intermittent arterial bleeding and may be extremely difficult to identify endoscopically when not actively bleeding. Most lesions occur in the stomach, with only 16% occurring in the small-bowel, most in the duodenum. Dieulafoy lesions are essentially normal vessels in an abnormal location within the submucosa. These abnormal arteries typically protrude through a small mucosal defect varying in size from 2 to 5 mm. They correspond to a type 2a lesion in the classification by Yano et al. [9], described endoscopically by those authors as a pulsatile red protrusion without surrounding venous distension. AVMs and AVFs result in an abnormal communication between a feeding artery and Fig. 4 Diagram shows proposed concept of development of cecal vascular ectasias. (Reprinted with permission from [14]) A, Normal state of vein perforating muscular layers. B, With muscular contraction or increased intraluminal pressure, vein is partially obstructed. C, After repeated episodes, submucosal vein becomes dilated and tortuous. D, Later, veins and venules draining into abnormal submucosal vein become similarly involved. E, Ultimately, capillary ring becomes dilated, precapillary sphincter becomes incompetent, and small arteriovenous communication develops. vein, causing high intralesional flow. These abnormalities may be accompanied by an enlarged feeding artery and early appearance of a draining vein. AVMs are most common in the brain and spinal cord and are thought to be congenital. Typically, colonic AVMs are congenital and are usually singular and large. The small AVMs seen in the gastrointestinal tract of older patients may have a different pathogenesis. Boley et al. [16] suggested that these lesions are acquired and evolve from the more common angioectasias following functional failure of the precapillary sphincter. In support of this concept, Boley et al. re- A Fig. 5 Angioectasia in 65-year-old woman with multiple episodes of melena. A C, Arterial (A), enteric (B), and delayed (C) phase axial images from multiphase CT enterography study show focal < 5-mm nodular area of enhancement in distal jejunum (arrow, B and C), undetectable on arterial phase and brightest on enteric phase. Angioectasia was subsequently ablated during balloon-assisted endoscopy. B C 68 AJR:201, July 2013

5 CT Enterography of Small-Bowel Vascular Lesions ported that an early draining vein was commonly seen at angiography in patients with vascular ectasias of the colon. Arterial lesions enhance most brightly during the arterial phase and may become invisible on enteric and delayed phases. Therefore, A A C failure to obtain arterial phase images during CT enterography may result in a missed diagnosis of these important lesions. A tiny nidus of enhancement on the arterial phase usually indicates the site of the lesion (Fig. 7). When associated with an early draining vein on the B B D Fig. 6 Small-bowel angiectasias. A, 70-year-old man with chronic blood-loss anemia and multiple small-bowel angioectasias. Coronal enteric phase image from multiphase CT enterography study shows focal bulbous swelling of intramural veins in wall of jejunum (arrows). B, Photomicrograph of resected colon segment in different patient shows narrowing of intramural vein passing through muscular layer (small arrow) with dilation of proximal segment (large arrow), which closely resembles CT appearance in figure 6A. (Reprinted with permission from [14]) arterial phase, the lesion most likely represents an AVM (Fig. 8). In the absence of an early vein, Dieulafoy lesions cannot be distinguished from AVFs or AVMs. Venous Lesions The most common venous lesions encountered during multiphase CTE for evaluation of obscure gastrointestinal bleeding are venous angiomas and small-bowel varices. Venous angiomas are rare lesions of the smallbowel that may occur in isolation or may be associated with Klippel-Trenaunay or blue rubber nevus syndrome. The lesions are classified pathologically as hamartomas and consist of large blood-filled sinuses lined by endothelial cells [17]. Small-bowel varices form within adhesions in the setting of mesenteric venous hypertension due to either mesenteric venous obstruction or portal hypertension. Adhesions between adjacent bowel loops or between the bowel and peritoneum provide a pathway for the varices to form. Small-bowel varices should be suspected in patients who have had prior abdominal surgery and have evidence of mesenteric venous hypertension [18]. Venous lesions enhance progressively usually nonenhancing on the arterial phase and enhancing more intensely during the enteric and delayed phases. The multiphase CTE appearance of small-bowel hemangiomas is similar to that of hepatic cavernous hemangiomas slow filling of the blood-filled sinuses resulting in progressive globular enhancement. In many of the hemangiomas we have encountered, phleboliths were present within the lesions and were best seen on the arterial phase Fig. 7 Dieulafoy lesion in 58-year-old man with hematochezia. A C, Arterial (A), enteric (B), and delayed (C) phase axial images from multiphase CT enterography study show small nodular area of enhancement in distal jejunum visible only on arterial phase (large arrow, A). Adjacent linear collection of contrast material (small arrow, A) may represent active bleeding. D, Superior mesenteric angiogram confirms finding of arterial nidus (arrow). AJR:201, July

6 Huprich et al. Fig. 8 Arteriovenous malformation in 44-year-old woman with hematochezia. Coronal maximumintensity-projection image from arterial phase shows arterial nidus (arrow) and early appearance of draining vein (arrowhead). before lesion enhancement occurs (Fig. 9). Varices may be visible on the enteric phase and become more intense on the delayed phase, with progressive filling of the mesenteric-systemic venous collateral veins (Fig. 10). Discussion Although there are many articles reporting the use of CTE in the detection of smallbowel neoplasms, there are few reports describing the use of CT in the diagnosis of small-bowel vascular lesions [19 21]. In our experience reviewing several thousand multiphase CTE studies in patients with obscure gastrointestinal bleeding, we have found multiphase CTE to be useful, not only in the detection of small-bowel vascular lesions but also in the categorization of these abnormalities. As a result of lesion characterization by multiphase CTE, appropriate treatment can be tailored to the specific vascular abnormality. For example, some arterial lesions may be more effectively treated with catheter embolization, whereas angioectasias may respond best to endoscopic treatment. The effect of lesion characterization by multiphase CTE on treatment strategies needs further evaluation. The major drawback of multiphase CTE is the significant patient radiation dose (equivalent to three single-phase CTE examinations approximately msv). Obviously, the dose can be reduced by eliminating one or two of the phases, but on the basis of our previous study, doing so significantly lowers sensitivity [22]. This reduced sensitivity is primarily the result of failure to detect arterial lesions when the arterial phase is eliminated. Failure to detect arterial lesions has grave clinical implications because these lesions are associated with a high risk of massive bleeding. The recent introduction of dose reduction techniques promises to offer significantly reduced patient dose without a loss of diagnostic accuracy [23]. Furthermore, this technique should be applied judiciously by insisting that patients undergo recent upper endoscopy and colonoscopy to exclude a bleeding source before performing multiphase CTE. We often triage younger patients, in whom the potential risk from radiation is higher, to CT systems with iterative reconstruction and kilovoltage selection software, or we may perform only arterial and enteric imaging, with radiologist review of images while the patient is on the scanner table. The detection of arterial and venous lesions by multiphase CTE is generally straightforward and accurate. On the other hand, because of the high prevalence in the nonbleeding population and common multiplicity of angioectasias, detection of clinically significant angioectasia using this technique is problematic. This situation is similar to endoscopy, in which angioectasias are commonly seen but, unless there are endoscopic signs of recent bleeding, the clinical significance of detecting a red spot is unknown. The introduction of wireless capsule endoscopy and balloon-assisted endoscopy has greatly advanced the care of patients with obscure gastrointestinal bleeding. Capsule endoscopy remains the preferred initial study in patients with obscure gastrointestinal bleeding at most institutions. The timing of capsule endoscopy related to bleeding is critical because the diagnostic yield of capsule endoscopy is highest at the time of bleeding. In cases of occult obscure gastrointestinal bleeding, it may be beneficial to perform multiphase CTE as the first study after negative upper endoscopy and colonoscopy, as proposed by Singh and Alexander [24]. Agrawal et al. [25] also reported CTE to be useful in cases of overt obscure gastrointestinal bleeding. In their study, A B C Fig. 9 Jejunal hemangioma in 38-year-old woman with blood-loss anemia. A C, Arterial (A), enteric (B), and delayed (C) phase coronal images from multiphase CT enterography study show phlebolith on arterial phase (arrow, A). Progressive globular enhancement is seen on enteric and delayed phase images (arrows, B and C). 70 AJR:201, July 2013

7 CT Enterography of Small-Bowel Vascular Lesions Fig. 10 Small-bowel varices in 56-year-old man with cirrhosis, mild portal hypertension, and recent episode of hematochezia. Enteric phase axial image from multiphase CT enterography study shows brightly enhancing tangle of veins (arrows) at site of prior small-bowel anastomosis. (Reprinted with permission from [30]) CTE was performed after a nondiagnostic capsule endoscopy and had a diagnostic yield of 50% in overt obscure gastrointestinal bleeding cases. Overall, multiphase CTE is complementary to capsule endoscopy and is better at detecting small-bowel tumors [5, 7, 24]. Balloon-assisted endoscopy is most often reserved as a therapeutic procedure after positive capsule endoscopy or multiphase CTE studies. Balloon-assisted endoscopy is capable of detecting angioectasias as well as treating these lesions, whether there are signs of bleeding or not. However, as previously discussed, balloon-assisted endoscopy is costly, has risk, and requires technical expertise that is available only at a limited number of medical centers. Balloon-assisted endoscopy can be performed antegrade or retrograde, or it can be performed with a combined antegrade and retrograde approach, allowing complete small-bowel visualization in about 30 60% of cases. Unfortunately, because of the multiplicity of angioectasias, recurrent bleeding after successful endoscopic treatment is frequent. Rebleeding after endoscopic treatment of small-bowel angioectasias at balloon-assisted endoscopy is approximately 50% at 2 3 years [26, 27]. Although bleeding from small-bowel vascular lesions accounts for significant morbidity and health care costs, in our experience, mortality is low compared with patients with small-bowel tumors because most symptomatic small-bowel neoplasms are malignant [28]. Therefore, it is imperative that techniques for the evaluation of obscure gastrointestinal bleeding accurately detect smallbowel tumors. We know from prior studies that enterography at referral medical centers may be superior to capsule endoscopy in the detection of small-bowel tumors [7, 29]. At our institution, multiphase CTE is the initial examination for obscure gastrointestinal bleeding, not only because of its ability to detect vascular lesion but also because of it superior performance in detecting small-bowel tumors, which are clinically the most important small-bowel pathology to identify. In our practice, patients with negative multiphase CTE usually undergo capsule endoscopy. Although further studies are needed, it is our opinion that multiphase CTE is superior to capsule endoscopy in the detection of small-bowel tumors but less sensitive for detecting vascular lesions. Balloon-assisted endoscopy is generally performed to define or treat an abnormality seen on multiphase CTE or capsule endoscopy. In select cases of severe obscure gastrointestinal bleeding with negative multiphase CTE and capsule endoscopy studies, balloon-assisted endoscopy should be performed beginning with the antegrade approach. The evaluation of patients with obscure gastrointestinal bleeding due to small-bowel vascular lesions remains challenging. The relative inaccessibility of the small-bowel to direct inspection combined with the complex variety of abnormalities responsible for obscure gastrointestinal bleeding further complicates the problem. Wireless capsule endoscopy and balloon-assisted endoscopy have greatly simplified these challenges. Multiphase CTE is a robust complementary technique that permits detection and characterization of small-bowel vascular lesions. Acknowledgments We acknowledge the encouragement of our longtime collaborators, J. G. 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