INTRODUCTION — Transabdominal ultrasonography is most commonly used to obtain images of hepatobiliary, urogenital, and pelvic structures. Its utility for imaging the alimentary gastrointestinal tract is less well established, principally because of technical difficulties in obtaining quality images of these regions. However, improvements in ultrasound technology and increasing familiarity with ultrasonographic findings in a variety of gastrointestinal disorders are broadening its applications. Society guidelines regarding the use of gastrointestinal ultrasound are available [1].
An advantage of ultrasound imaging compared with endoscopy and contrast radiography is that it permits evaluation of the transmural aspects of inflammatory or neoplastic pathology within its surrounding structures [2]. This can provide an important contribution for diagnosis and monitoring of disease activity. Other advantages are that it is widely available, noninvasive, can be performed without preparation, and lacks radiation exposure (which may be particularly desirable in patients such as pregnant women) [3,4].
On the other hand, important limitations of ultrasonography are that the alimentary tract cannot be visualized over its entire length, many of the findings are nonspecific, and obtaining and interpreting the images is operator-dependent. Furthermore, ultrasound is far less useful in patients with obesity in whom high-frequency scanning may not be possible.
This topic review will provide an overview of transabdominal ultrasonography of the small and large bowel, while summarizing its use in a variety of gastrointestinal disorders.
Society guidelines and position papers on gastrointestinal ultrasound have been published, and our approach is generally consistent with society guidance [3,5-8].
TECHNICAL CONSIDERATIONS — Imaging of the alimentary tract requires high-frequency (5 to 17 MHz), high-resolution linear or convex array transducers, a great deal of scanning experience, and patience. The standardized evaluation should optimally take place preprandially since images from filled intestines can be difficult to interpret, particularly when motility is being evaluated. On the other hand, under emergency conditions, such as ileus (eg, due to obstruction, an incarcerated hernia, or intussusception), appendicitis, or diverticulitis, the exam may be performed postprandially.
The ileocecal region and the sigmoid colon can be identified by ultrasound imaging in most patients. Landmarks in the ileocecal region are the right iliac artery and vein, while landmarks in the sigmoid region are the left iliac artery and vein. The remaining colonic segments can also be evaluated adequately by continuous scanning in many patients. The rectum and distal parts of the colon cannot always be displayed satisfactorily.
Intestinal wall thickness and sonomorphology — A central element of alimentary tract imaging is the correct estimation of intestinal wall thickness. A number of different reference values for defining normal have been proposed (ranging from 1 to 5 mm). In our experience, the normal intestinal tract thickness in the terminal ileum, cecum, and right and left colon is <2 mm when examined with graded compression in adults [9-11] and children [12,13]. It is important to appreciate that a contracted intestinal segment can be misinterpreted as a thickened wall. In addition to the wall thickness, its overall echo texture and appearance within surrounding structures should be considered when interpreting the results.
High-resolution transducers usually permit visualization of the five layers of the colonic and stomach walls (table 1) [14,15]. Imaging of the walls of the small intestine usually requires it to be filled with liquid. The small and large intestines can be distinguished by scanning the haustra of the colon and the circular folds of Kerckring in the small intestine [16]. In unclear cases, scanning of the intestines during various filling stages can be helpful. The specific appearance of these features can also help to establish a diagnosis. As an example, widening of the spaces between the Kerckring folds can be seen in patients with villous atrophy (such as celiac disease).
Assessment of abdominal lymphadenopathy — Conventional ultrasound can be used to evaluate abdominal lymph nodes (LNs). It has the advantages of high-resolution, real-time evaluation, and relatively low cost. Methods such as elastography can help identify benign versus malignant lymph nodes [17]. Indications for transcutaneous ultrasound (TUS) and endoscopic ultrasound (EUS) include the detection and characterization of lymph nodes and guidance for LN biopsy [18,19]. Advances in ultrasound technology, such as contrast-enhanced ultrasound (CEUS), contrast-enhanced endoscopic ultrasound (CE-EUS), and real-time elastography, show potential to improve the accuracy of ultrasound for the differential diagnosis of benign and malignant lymph nodes. As with TUS and EUS, CEUS and CE-EUS have been used for the guidance of fine-needle aspiration and assessment of treatment response [18].
Color Doppler imaging — A number of authors have described the utility of color Doppler imaging during standard ultrasound examination in a variety of gastrointestinal disorders, particularly in patients with Crohn disease [20-27], celiac disease [28-33], and mesenteric artery stenosis [34-38]. However, experience with these imaging modalities is limited, and their accuracy has not been well defined [39,40]. As a result, their role in diagnosis of or in monitoring disease activity remains unclear. A promising approach is combining mesenteric inflow by Duplex scanning (systolic and diastolic velocities, resistance index) with visualization of the end-organ vascularity by color Doppler imaging [41].
●Acute inflammation of the intestinal wall (such as in patients with Crohn disease) is accompanied by increased perfusion of the mesentery, which can be displayed non-quantitatively with color duplex, with or without the administration of echo-enhancing agents (CEUS using agents such as SonoVue). In patients with Crohn disease, the perfusion pattern may facilitate differentiation of inflammatory from cicatricial-fibrostenosis and a correlation with endoscopically active Crohn disease [42]. However, technical factors (eg, depth of penetration, pressure, and equipment used) may influence the ability to make this distinction [43,44]. (See 'Contrast-enhanced ultrasound (CEUS)' below.)
●Mesenteric Doppler ultrasonography has been advocated as a reasonably accurate screening modality for the detection of high-grade superior mesenteric artery stenoses. Sensitivity exceeding 90 percent and a negative predictive value of close to 99 percent has been reported in patients with more than a 50 percent stenosis of the superior mesenteric or celiac arteries. As a result, it is reasonable to pursue other etiologies of abdominal pain after a negative study. A positive study should be followed by angiography, which can further establish the feasibility of revascularization. (See "Chronic mesenteric ischemia".)
Contrast-enhanced ultrasound (CEUS) — CEUS uses echo-enhancing agents such as SonoVue (which contains sulphur hexafluoride). In patients with Crohn disease, CEUS enables quantification of bowel wall vascularity [45], however, whether this correlates well with histologic findings is unclear [46,47]. (See "Contrast echocardiography: Contrast agents, safety, and imaging technique", section on 'Second-generation contrast agents'.)
CEUS can also be used to evaluate disease activity in inflammatory bowel disease because it can visualize microvascularity of the tissue surrounding the intestines [48]. In patients with inflammation, three bowel wall perfusion patterns are seen with CEUS: submucosal enhancement, inward transparietal enhancement, and outward transparietal enhancement [42]. Disease activity can be further quantified using time intensity curve analysis [49,50]. The quantitative measurements of bowel enhancement obtained by CEUS have been shown to correlate with endoscopic severity and histopathologic findings [51,52]. CEUS may also be effective in the recognition of predominantly cicatricial stenoses in patients with Crohn disease [53]. Finally, CEUS can be used as part of the evaluation for postoperative recurrence of Crohn disease [54].
Use of CEUS to evaluate inflammatory bowel disease activity and other conditions of the gastrointestinal tract is discussed separately. (See "Contrast-enhanced ultrasound: Gastrointestinal applications outside of the liver", section on 'Gastrointestinal tract'.)
There are reports of off-label extravascular or intracavitary administration of ultrasound contrast agents (UCA) to improve sonographic assessment. No standard dosage of UCA has been established so far for intracavitary injection. The range reported is 0.1 to 1 mL SonoVue (most commonly just a few drops) diluted in 10 mL or more of 0.9 percent saline; a higher content of SonoVue may be needed for high-frequency ultrasound probes. CEUS detection and classification of fistulas, whatever the initial disease, has been proven to be effective. In principle, UCA can be instilled into any sonographically accessible physiologic or pathologic body cavity to assess morphology of the cavity and potential communications with adjacent structures or organs. Clinical applications include evaluation of abscesses [55], intestinal and other fistulas [56], gastroesophageal reflux and hiatal hernia [57,58], the gastric lumen, Zenker's diverticulum [59], and intestinal stenoses [60,61].
Elastography — Elastography is a noninvasive method in which tissue stiffness can be imaged as a color map or shear wave velocity. The ultrasound probe is used to palpate the tissue. It is usually done transcutaneously but can be applied intraoperatively or via an endoscope [62]. The tissue deformation produced (ie, strain) is assessed by following the way the speckle in the image moves, usually with a tracking algorithm that analyzes the radio-frequency data. The data can then be used to form an image that is coded in color or grayscale to show the pattern of strain, which is inversely related to tissue stiffness. Therefore, strain elastography (SE) allows assessment and visualization of relative elasticity differences. The area to be evaluated is defined by a region of interest in a similar way to color Doppler imaging [18,63,64]. SE may show the layered structure of the gastrointestinal wall. SE is used to assess the firmness of focal lesions of the gastrointestinal tract [60]. SE can help determine if a stenosis is caused by inflammation or fibrosis since fibrotic stenoses appear stiff and inflammatory stenoses appear soft [65,66]. Furthermore, patients with active Crohn disease have a higher strain ratio between the inflamed and normal regions than patients in remission [67]. In a study on inflammatory bowel disease, the findings on elastography were significantly correlated with the endoscopic findings [68]. Ultrasound elastography has been used as a technique for differentiating fibrosis from inflammation [69]. (See "Noninvasive assessment of hepatic fibrosis: Ultrasound-based elastography", section on 'Principles behind ultrasound-based elastography'.)
ADDITIONAL SONOGRAPHIC EXAMINATION TECHNIQUES — A number of modifications of standard ultrasound techniques continue to be developed:
●One of these, hydrocolonic ultrasonography, involves the retrograde instillation of water into the colon, which helps to provide excellent images of the colonic wall morphology [70-72]. However, its clinical utility is unclear.
●Transrectal, transvaginal, and other perineal ultrasound techniques can provide detailed information about perineal structures [73]. We have found these approaches to be particularly helpful in the initial evaluation of patients with perineal fistulas [74]. However, they are of limited value in patients with deep or complex fistulas [75,76]. Although endorectal ultrasound with elastography can quantify anal sphincter elastic properties, its role in the evaluation of patients with fecal incontinence is unclear [77,78].
●Point of care ultrasound has been studied using small, handheld ultrasound devices with promising results [79].
APPENDICITIS — Ultrasonography has been used successfully in diagnosing acute appendicitis primarily in children, but also in adults [7,80,81] (table 2). (See "Acute appendicitis in adults: Clinical manifestations and differential diagnosis" and "Acute appendicitis in children: Diagnostic imaging" and "Acute appendicitis in adults: Diagnostic evaluation".)
The normal outer appendiceal diameter (with and without) compression was measured in 205 consecutive children without clinical signs of appendicitis, [82]. The mean age of the children included in the study was nine years. The appendix was visualized in 142 of 205 children (69 percent). The mean appendiceal diameter without and with compression was 4.2±0.9 mm and 3.5±0.8 mm, respectively, with 54 percent of the appendices appearing in the mid-pelvic location. Age, weight, and height all affected the visualization rate of the normal appendix.
Sonographic signs of appendicitis include (image 1 and image 2):
●Noncompressible appendix with a diameter of >6 mm
●Focal pain over appendix with compression
●Appendicolith
●Changes of echogenicity (which might be hyper- or hypoechoic) of inflamed periappendiceal fat
●Fluid in the right lower quadrant
In a retrospective review of 304 consecutive patients, the highest sensitivity (99 percent) and specificity (95 percent) for making a diagnosis of appendicitis were a mean outer diameter of ≥7 mm or wall thickness >1.7 mm, resulting in one (0.5 percent) false-negative and six (3 percent) false-positive studies [83].
In some patients, the whole length of the appendix (up to 10 cm or more) can be visualized. Obstruction of the appendix (eg, by an appendicolith, neoplasia or, in endemic areas, parasites) can be identified in some patients.
Inflammation of the appendiceal wall may be followed by localized ischemia (which may be visualized by color Doppler imaging) and necrosis. Complications of acute appendicitis (perforation and abscess formation with or without generalized peritonitis and pylephlebitis) can also be detected during ultrasonography.
EPIPLOIC APPENDAGITIS — Epiploic appendagitis (also known as appendicitis epiploica) is a rarely recognized disease of the colonic epiploicae [84-93]. Its main clinical feature is acute abdominal pain that is often mistaken for appendicitis or diverticulitis.
On abdominal ultrasound, the inflamed appendage appears as a noncompressible, solid, hyperechoic ovoid mass with a subtle hypoechoic rim located at the point of maximal tenderness. The inflamed fatty mass is fixed to the colon and often also to the parietal peritoneum during inspiration and expiration. Doppler studies typically reveal absence of blood flow in the appendage and normal blood flow in the hyperechoic inflamed fat surrounding the appendage. (See "Epiploic appendagitis", section on 'Abdominal ultrasound'.)
Contrast-enhanced ultrasound may show a central area of no enhancement with moderately increased vascularization around the avascular necrotic appendage [94]. The transverse colon is rarely involved. Ultrasonography can establish the diagnosis [95], although computed tomography is more commonly used.
DIVERTICULITIS — The diagnosis of diverticulitis is usually established based upon the history, physical examination, and the results of imaging tests, most commonly computed tomography scanning. However, high-resolution, graded, compression ultrasonography continues to be widely used in many centers to evaluate patients with suspected diverticulitis [96,97]. Reported sensitivities range from 84 to 98 percent and specificities from 80 to 99 percent (table 3) [98-106] (see "Clinical manifestations and diagnosis of acute colonic diverticulitis in adults"). It can also be used to assess the resolution of the disease.
Typical ultrasonographic features seen in patients with acute diverticulitis include:
●A hypoechoic peridiverticular inflammatory reaction.
●Mural and peridiverticular abscess formation with or without gas bubbles.
●Bowel wall thickening (segmental mural thickening greater than 3 to 4 mm) at the point of maximal tenderness.
●Normal-appearing diverticula in the surrounding segments.
●A prominent muscularis layer (a general feature of diverticulosis). The lamina muscularis propria is thickened due to hypertrophy. This is a "working" hypertrophy of the muscle layer in diverticulosis and does not correspond to inflammation. Occasionally, a triple layering of the lamina muscularis propria can be recognized: the inner circular fibers, a thin membrane of collagenous fibers, and the outer longitudinal muscle fibers.
Ultrasonography can also identify the major complications of diverticulitis, including obstruction, peritonitis (with ascites and sometimes diffuse peritoneal thickening and scattered loculated fluid collections), and fistula and abscess formation (image 3). Fistulas appear as hypoechoic areas next to inflamed diverticula with extraluminal air bubbles extending in the bladder, vagina, or abdominal wall.
Once the diagnosis has been established, ultrasonography can be used to facilitate percutaneous drainage of localized abscesses, thereby downstaging complicated diverticulitis, avoiding emergency surgery, and permitting single stage elective surgical resection. (See "Acute colonic diverticulitis: Triage and inpatient management".)
CROHN DISEASE — Transabdominal ultrasonography is useful for the detection of bowel wall thickening and for determining the extent of involved segments in active Crohn disease (image 4) [107,108]. Ultrasound reliably depicts both bowel-related and mesenteric features of Crohn disease, and ultrasound findings correlate strongly with magnetic resonance enterography (MRE) findings [109].
Several studies comparing the value of ultrasonography with endoscopic and radiologic results in Crohn disease have found a sensitivity between 73 and 96 percent and a specificity between 90 and 100 percent (table 4 and table 5) [72,110-132]. Sonographic features of the colon include (asymmetric) segmental bowel wall thickening corresponding to endoscopic signs of disease activity, namely ulcerations, edema, hyperemia, and polypoid mucosal changes with pathologically thickened skip areas adjacent to areas of normal-appearing mucosa (cobblestone appearance). This pattern is different from the continuous involvement observed in ulcerative colitis, which can also be identified by ultrasonography (table 6) [72,118-120,133].
For ultrasound assessment of disease activity, the Simple Ultrasound Score for CD (SUS-CD) was developed. The score ranges from 0 to 5 based on bowel wall thickness (<3.0 mm = 0; 3.0 to 4.9 mm = 1; 5.0 to 7.9 mm = 2; ≥8.0 mm = 3) and color Doppler signals (no or single vessel = 0; 2 to 5 vessels per cm2 = 1; >5 vessels per cm2 = 2). The SUS-CD score correlated well with the Simple Endoscopic Score for CD in endoscopic imaging [134].
Intestinal ultrasound (IUS) may be used to predict and monitor response to IBD treatment [135-144]. When monitoring therapy with IUS, we use the same type of probe (high frequency or abdominal probe) and device settings (Doppler scale, presets) during each examination. The treatment response rate assessed by IUS has been comparable to assessments with endoscopy and magnetic resonance enterography [135].
A treatment response has been defined as a reduction in bowel wall thickness by more than 25 percent, >2 mm, or >1 mm with a decrease in color Doppler signals [135]. Transmural healing has been defined as a bowel wall thickness ≤3 mm [143,145].
In addition, there are other parameters such as normalization of vascularization by Doppler US, normal bowel wall stratification, absence of mesenteric fat hypertrophy, lymph node enlargement, and disease complications (ie, strictures, fistulas) [144,146]. As an example, transmural remission by IUS has been described as bowel wall thickness ≤3 mm with normal color Doppler signals [135].
A consensus panel has developed a standardized method for reporting IUS results [145,147].
Lymph node enlargement is a common ultrasonographic finding in patients with Crohn disease (25 percent of 240 patients in one series [148]). In one report, lymph node enlargement was more frequent in young patients and in the presence of septic complications such as fistulas and abscesses [148]. The finding of lymph node enlargement was of limited valued in assessing disease activity.
Ultrasonography can also detect complications such as fistulas (image 5), abscesses, carcinoma, and ileus. As discussed above, the addition of color Doppler imaging can help to distinguish active disease from a post-inflammatory stricture. Estimates of the sensitivity and specificity of ultrasonography for detecting fistulas have ranged between 50 to 89 and 90 to 95 percent, respectively [149]. Estimates of the sensitivity and specificity for detecting abscesses have ranged between 71 to 100 and 77 to 94 percent, respectively [121,133,150-152].
A prospective study suggested that routine ultrasonography in patients with Crohn disease can reveal unexpected pathologic findings that have therapeutic implications [153]. The study included 255 patients with Crohn disease who underwent regular ultrasonography irrespective of symptoms and disease activity. Patients with abnormal findings underwent further evaluation with additional radiologic and endoscopic imaging and treatment as needed.
Of 17 patients with inactive disease, ultrasonography revealed four with an enteroenteric fistula, seven with a mesenteric or perirectal fistula, and six with transmural mesenteric inflammation without a fistula. Ultrasonography of the remaining abdominal organs revealed pathological findings with further diagnostic implications in 25 of 255 (10 percent) patients and with therapeutic implications in 9 of 255 (4 percent).
ULCERATIVE COLITIS — The diagnosis of ulcerative colitis is usually established by the patient's history and typical endoscopic appearance of the mucosa and histology. (See "Clinical manifestations, diagnosis, and prognosis of ulcerative colitis in adults".)
Treatment is based in part upon the extent of disease. Thus, it is useful at the initial presentation to document the extent of inflammation, which can be accomplished by combining flexible sigmoidoscopy and ultrasonography. Early sonographic signs of active ulcerative colitis include a thickened hypoechoic mucosa layer, corresponding to the endoscopic findings of engorgement of the erythematous mucosa with petechiae, exudates, and friability. More severe cases may be associated with transmural bowel wall thickening corresponding to the endoscopic findings of exudates and ulcerations (image 6). Patients with fulminant disease may have sonographically transmural inflammation, an appearance similar to Crohn disease.
Although transmural inflammation is not a feature of ulcerative colitis, some studies have demonstrated changes in bowel wall thickness. In one study, intestinal ultrasound (IUS) showed moderate agreement with colonoscopy for assessing disease activity in all colon segments except the rectum [154].
Thickening of the bowel wall and the presence of vascularization on color Doppler are two criteria that have correlated well with endoscopic activity in UC. These criteria have been summarized as the Milan Ultrasound Criteria (MUC) and may be used to assess disease activity [155].
However, the clinical and sonographic findings at initial presentation and during exacerbations are not specific to ulcerative colitis, and may be seen in a number of other disorders, including colitis due to drugs (such as nonsteroidal antiinflammatory drugs, retinoic acid, gold, and possibly oral contraceptives), infectious colitis (due to Clostridioides [formerly Clostridium] difficile, Salmonella, Shigella, Campylobacter, Aeromonas, and Escherichia coli O157:H7), and other chronic inflammatory bowel diseases (such as Crohn disease and ischemic colitis) [156]. The differential diagnosis is broader in patients who are immunocompromised. Thus, sonographic findings should be used to complement other clinical and laboratory features of the presentation.
INFECTIOUS ENTEROCOLITIS — Various bacteria are associated with acute infectious enterocolitis. The most frequently encountered agents include Salmonella, Campylobacter, and Yersinia species, and enteropathogenic and enterohemorrhagic E. coli. Shigellosis is uncommon in Europe and the United States [157,158]. (See "Approach to the adult with acute diarrhea in resource-abundant settings".)
The sonographic differentiation of individual bacterial infections is not possible, although the images obtained may point toward the final diagnosis. All forms of secretory small bowel derived diarrhea can initially present with a fluid-filled small bowel [159]. Most of these infections are associated with intestinal wall thickening, with preservation of the wall layers (image 7) [2,159-163]. Prominent mesenteric lymph nodes are frequently seen (table 7).
●Salmonella enteritis – The pathogenesis of diarrhea in Salmonella gastroenteritis results from complex interactions between bacterial products and host cells. Salmonellae selectively attach to specialized epithelial cells overlying Peyer's patches in the colon known as M cells [164]. These cells are an important portal of entry of Salmonellae and other pathogens into the submucosal lymphoid system. Involvement of the submucosal lymphoid system explains the occasional disparity between the sonographic findings of a thickened bowel but with endoscopically normal-appearing mucosa [162,165-170]. Thickening of the mucosa with a feathery appearance is typical [171]. (See "Nontyphoidal Salmonella: Gastrointestinal infection and asymptomatic carriage".)
●Campylobacter enteritis – The diagnosis of Campylobacter enteritis (either as a small bowel or large bowel pathogen) cannot be made on clinical and sonographic grounds alone. However, the presence of severe abdominal pain with diarrhea and sonographic findings of ileocecitis may suggest the diagnosis [162,168,169,172].
●Yersiniosis – Although there are no distinct clinical, radiologic, or hematologic findings that are pathognomonic for Yersiniosis, sonographic findings of ileocecitis may be suggestive, especially in patients with mesenteric lymphadenopathy. However, lymph nodes are almost always enlarged with other bacterial infections as well. Another suggestive finding is thickening of the distal ileum, which corresponds to the presence of the dense inflammatory infiltrate, which is typical of Yersiniosis [159-162,168,169,173,174].
●Enterohemorrhagic E. coli – Enterohemorrhagic E. coli, most notably E. coli O157:H7, is a relatively common, but probably under-recognized, cause of infectious colitis. Sonographic signs include thickening of the bowel wall, especially the right colon. The sonographic diagnosis of colitis without identifiable infectious agents should raise suspicion for the infection, whose confirmation requires specialized cultures that may not be performed as part of routine stool cultures. (See "Shiga toxin-producing Escherichia coli: Microbiology, pathogenesis, epidemiology, and prevention".)
●Shigella – Shigella is the classic cause of colonic or dysenteric diarrhea, mostly documented as a foodborne disease. As few as 10 organisms can initiate disease, and person-to-person spread is feasible. Ultrasonography may show signs similar to ulcerative colitis. (See "Shigella infection: Treatment and prevention in adults".)
●Vibrio cholerae – V. cholerae infection is uncommon in Europe and the United States. This organism is associated with small bowel diarrheal illnesses. Sonographically detectable bowel wall thickening is rarely recognized but may be prominent in patients with severe disease with edema of the bowel wall. Fluid-filled small bowel due to secretory mechanisms induced by the toxin may be the only sonographically detectable sign.
●Intestinal tuberculosis – The incidence of intestinal tuberculosis increased with the AIDS pandemic. As with Crohn disease, all regions of the intestine may be involved, although the ileocecal region is affected in up to 90 percent of patients. Both sides of the ileocecal valve are typically inflamed, preventing it from closing satisfactorily [175].
The ultrasound image displays a hypoechoic (sometimes asymmetrically thickened) mucosa with loss of folds and unclear demarcation from (sometimes asymmetrically) thickened submucosa, so that a pseudo-polypoid image prevails. Short stenoses, mesenteric hyperechoic inflammatory signs, fistulas, and abscesses can be seen on the ultrasound image. Other characteristic signs include severe mesenteric lymphadenopathy (sometimes more than 10 hyperechoic round to oval-shaped lymph nodes are detected) and a distended ileocecal valve, with asymmetric (sometimes tumorous) thickening, especially affecting the medial cecal wall. Patients with peritoneal tuberculosis may also have ascites and thickening of the peritoneum.
The differential diagnosis includes Crohn disease, lymphoma, carcinoma of the cecum, and amebiasis. Less common diseases such as syphilitic gummas of the cecum, actinomycosis, or other opportunistic infections (eg, cytomegalovirus [CMV] infection, or atypical mycobacterial infection) can also produce similar sonographic findings.
●Whipple's disease – Whipple's disease is characterized by accumulation of macrophages in the lamina propria with intensely PAS-positive intracellular material. The etiologic agent was identified in 1992 as Tropheryma whipplei, which is closely related to many other soil-borne actinomycetes. (See "Whipple's disease".)
Ultrasonography may reveal duodenal and small bowel wall thickening due to edema [176], ascites, and mesenteric lymphadenopathy [177-183]. Whipple's disease appears sonographically similar to intestinal Mycobacterium avium complex (MAC) infection in patients with AIDS presenting the so-called "white bowel" caused by intestinal lymphedema [184].
●Virus-related enteritis – Rotaviruses [185,186], norovirus (Norwalk agent), enteric adenoviruses, astroviruses, and coronaviruses are among the leading causes of diarrhea in children. Fluid-filled small bowel due to secretory mechanisms may be the only sonographically detectable sign.
However, we avoid performing intestinal ultrasound in patients with norovirus because the examination is generally not necessary and should be avoided to prevent viral transmission. (See "Norovirus".).
●Cytomegalovirus colitis – Typical sonographic features of CMV infection include hypoechoic transmural thickening (similar to Crohn disease) accompanied by a hyperechoic mesenteric inflammatory reaction. Although the entire intestine may be affected [187], special attention should be given to the ileocecal region, the ascending colon, and the duodenum in immunocompromised patients.
The exact cause of the above sonographic features is unclear. One possibility is that the changes are the result of occlusive vasculitis, which could explain similarities with Crohn disease. CMV lesions of the intestinal wall are often found in conjunction with mucosal Kaposi's sarcoma in patients with HIV infection. By ultrasound image, Kaposi's sarcoma is often detected as a hypoechoic enlargement of the mucosa with a distinct delimitation from the submucosa.
●Giardia lamblia – Sonographic changes in the development of G. lamblia infection are nonspecific. Thickening of the intestinal wall does not occur. Patients who have developed significant malabsorption may have a liquid-filled jejunum/ileum with hypermotility. Sonographic detection of nonenlarged mesenteric lymph nodes (<17 mm) with normal echogenicity may occasionally be seen. (See "Giardiasis: Epidemiology, clinical manifestations, and diagnosis".)
●Amebiasis – Amebic colitis, with its various signs and extraintestinal manifestations, cannot be distinguished sonographically from other inflammatory diseases of the colon [188,189]. Nevertheless, suggestive sonographic findings (eg, an ameboma or a liver abscess) should be sought.
●Cyclospora – Cyclospora cayetanensis is another cause of infectious diarrhea that has been identified in both sporadic cases and in outbreak settings. Sonographic signs are nonspecific, with fluid-filled small bowel in the absence of bowel wall thickening. (See "Cyclospora infection".)
ANTIBIOTIC-ASSOCIATED COLITIS — Most patients with antibiotic-related diarrhea do not have colitis, and thus have no detectable sonographic abnormalities. On the other hand, patients who develop pseudomembranous colitis, or much less commonly, penicillin-induced colitis, may have sonographic abnormalities [157,158].
Pseudomembranous colitis — The most common finding in patients with pseudomembranous colitis caused by C. difficile is symmetric mucosal and submucosal wall thickening, which is often most prominent in the left colon [190-199]. However, sonographic findings are insufficiently specific to distinguish pseudomembranous colitis from other bacterial causes of colitis (table 8) [191,200,201]. In severe cases, the colonic wall thickening is asymmetric and may resemble an intestinal lymphoma (image 8). Other sonographic features of severe infection include transmural inflammatory reactions, free pericolic fluid, and intramural gas echoes.
Penicillin-induced segmental hemorrhagic colitis — A characteristic sonographic feature of penicillin-induced segmental hemorrhagic colitis is the appearance of partially asymmetric wall thickening of the colon (typically in the right colon) with loss of intestinal wall layers due to edema and bleeding (table 8) [191,200-202]. Relative hypovascularization can be detected with color Doppler ultrasound examination. The surrounding colon may appear normal.
NEUTROPENIC ENTEROCOLITIS — Neutropenic enterocolitis (typhlitis) is a potentially fatal complication of severe neutropenia [203-205]. It typically affects the ileocecal region, which on ultrasound may reveal a distinct hyperechoic edematous hemorrhagic thickening of the intestinal wall. The presence of intramural gas and pericolic free fluid should raise concerns about imminent perforation. (See "Neutropenic enterocolitis (typhlitis)".)
ACUTE GRAFT VERSUS HOST DISEASE — Acute graft versus host disease (aGvHD) of the gastrointestinal tract is one of the major complications of allogeneic hematopoietic cell transplantation. Conventional B-mode ultrasonography and color Doppler imaging were used in combination to assess the extent, severity, course and prognosis of aGvHD of the gastrointestinal tract in 12 patients with suspected intestinal and/or severe cutaneous aGvHD [41,206]. The structure and thickness of the bowel wall and blood flow pattern in the superior mesenteric artery and bowel wall were useful for detection of aGvHD even before symptoms developed. All patients had thickened bowel wall segments, particularly in the ileocecal region. Four patients had ischemic bowel wall lesions as evidenced by a high-resistance flow pattern in the superior mesenteric artery; these patients did not respond to immunosuppressive therapy and ultimately died. Intestinal biopsy and histologic confirmation maybe necessary to confirm a diagnosis of aGvHD. A multiparametric approach has been proposed [207]. (See "Clinical manifestations, diagnosis, and grading of acute graft-versus-host disease".)
CYSTIC FIBROSIS — Stenosing fibrosis of the colon in association with cystic fibrosis was first described in 1994 [208]. Its pathogenesis is controversial [208-215]. One hypothesis is that the fibrosis is due to use of high doses of pancreatic enzymes. However, similar intestinal wall changes have also been observed in patients who were not taking pancreatic enzymes. Furthermore, stenosing fibrosis has not been described in patients taking high doses of pancreatic enzymes for other disorders (such as alcohol-related pancreatitis).
The characteristic ultrasound image shows the accentuation and thickening of the submucosa, which appears echogenic. Intestinal wall thickening is mainly found in the cecum and, slightly less pronounced, in the ascending colon, hepatic flexure, and the terminal ileum [216,217]. These changes are seldom detected in the sigmoid or distal colon. Other findings include distal intestinal obstruction syndrome, intussusception, and mucocele of the appendix.
INTUSSUSCEPTION — The classic ultrasound image of intussusception is a "bull's eye lesion," representing layers of the intestine within the intestine [167,215,216,218-221]. In addition, a lack of perfusion in the intussusceptum detected with color duplex imaging may indicate the development of ischemia [222-225].
CELIAC DISEASE — The main feature on ultrasound suggesting celiac disease is widening of the spaces between the Kerckring's folds (table 9 and table 10) [226-228]. Other suggestive features include dilation (>25 mm) of the affected jejunal loops with irregular, "looser-appearing" Kerckring's folds, a distinct increase in fluid content vivid peristalsis, and mesenteric lymphadenopathy. In addition, gas and chyme within the intestinal lumen may produce coarse hyperechoic images, like laundry in the drum of a washing machine (hence the term "laundry phenomenon") [8]. As a result, it can be extremely difficult to obtain sharp pictures of the enteral content [226]. The laundry phenomenon is a typical finding in disorders associated with villous atrophy.
Wall thickening of the intestinal wall is usually not observed. Exceptions are patients with hypoalbuminemia, who may have edematous wall thickening similar to that seen in patients with vasculitis [176].
Mesenteric lymph nodes are usually less than 17 mm and have an echo pattern similar to that of the liver [200]. An increased size of the lymph nodes, irregular echogenicity, or a cluster-like distribution pattern may indicate the development of an intestinal lymphoma. Much less frequently, ultrasonography may reveal the development of carcinoma of the small intestine.
BENIGN AND MALIGNANT TUMORS OF THE SMALL AND LARGE INTESTINE — Adenocarcinomas, neuroendocrine tumors, B-cell lymphoma, metastases (image 9), and benign tumors of the small intestine are infrequent. The gastrointestinal tract is the most common extranodal site for malignant lymphomas. These can be primary lymphomas originating in the small intestine or secondary involvement of a primary nodal non-Hodgkin lymphoma. Lymphomas arising in the intestine and associated with celiac disease are T-cell lymphomas. The sonographic appearance is usually that of a hypoechoic mass emanating from the intestinal wall [229-233]. The sonographic diagnosis of gastrointestinal stromal tumors has been reported [234,235]. Hematomas of the intestinal wall cannot be reliably differentiated from tumors.
Polyps, colon cancers, neuroendocrine tumors, and metastases appear on ultrasonography as hypoechoic masses. However, their identification can be difficult. Although mesenteric lymph nodes may be seen, the sensitivity and specificity of transabdominal ultrasonography is insufficient to be used for staging.
ISCHEMIC COLITIS — Ultrasonography, including color duplex imaging, can facilitate the identification of ischemic-hemorrhagic and secondary inflammatory or necrotic thickenings of the intestinal wall in patients with ischemic colitis [34,35,38,236-246]. The presence of color Doppler signals does not exclude ischemic colitis. A slightly symmetrical hypoechoic wall thickening is often an indication of the nonobstructive form of ischemic colitis with chronic compensated changes. In contrast, asymmetric wall thickening with an ileus may be seen in patients with acute mesenteric ischemia.
MESENTERIC ISCHEMIA — Acute mesenteric ischemia refers to the sudden onset of small intestinal hypoperfusion, which can be due to occlusive or nonocclusive obstruction of the arterial blood supply or obstruction of venous outflow [247]. Thromboses of the mesenteric veins may occur in patients with coagulation disorders or an inflammatory process [248]. (See "Overview of intestinal ischemia in adults".)
Ultrasound examination in patients with suspected mesenteric ischemia includes Doppler ultrasound (US) of the large mesenteric arteries and veins, as well as high-resolution examination of the bowel using duplex or power Doppler sonography and, if necessary, contrast-enhanced US [249,250]. Duplex imaging evaluates the velocity profile in the celiac trunk and the superior and inferior mesenteric arteries. Color duplex and, in some cases, additional echo-enhancing agents may be helpful for evaluating intestinal wall perfusion and identifying the mesenteric vessels. Systolic velocities of >250 to 300 cm/s are sensitive indicators of severe mesenteric arterial stenosis. However, the clinical significance of these findings is uncertain because ultrasonography does not assess collateral circulation (which often requires angiography). If superior mesenteric artery occlusion is not localized near its exit from the aorta, it may not be detected by Doppler sonography. (See "Overview of intestinal ischemia in adults" and "Acute mesenteric arterial occlusion".)
Ischemic bowel segments appear as hypoechoic, hypoperistaltic, thickened bowel wall without any stratification. A small bowel obstruction may coexist. Intestinal wall thickening occurs more frequently with venous thromboses than with arterial occlusions. In patients with small bowel gangrene, the small bowel wall is usually not thickened, but it appears very thin. If there is clinical suspicion, we look for intraluminal air pockets with a high-resolution linear transducer [251]. At the same time, pylephlebitis with air reflexes is often visible in the portal vein, its branches, and diffusely distributed in the liver parenchyma [252-254]. If the ischemia is reversible, the intestinal wall vascularization can be detected again in the repair stage.
AMYLOIDOSIS — Ultrasound features in patients with amyloidosis of the small intestine include asymmetric circular bowel wall thickening with distinct deposits (submucosal masses) with diminished peristalsis and dilatation [2,255-258]. (See "Gastrointestinal amyloidosis: Clinical manifestations, diagnosis, and management".)
VASCULITIS — Most patients with gastrointestinal manifestations of a systemic vasculitis have other symptoms suggesting the diagnosis (see "Overview of and approach to the vasculitides in adults"). Imaging studies, such as ultrasonography, computed tomography scanning, or barium studies, are frequently normal. When they are abnormal, they usually have nonspecific findings such as a thickened, edematous bowel wall [176] unless mesenteric infarction has occurred.
The sequelae of systemic vasculitis involving the gastrointestinal tract are usually due to inflammation and mesenteric ischemia, which may be identified by color Doppler ultrasonography. The onset of clinical manifestations may be acute and severe (eg, mesenteric infarction) or chronic. Chronic mesenteric ischemia may be associated with a variety of sonographic findings including bowel wall thickening and small bowel obstruction secondary to strictures, resembling Crohn disease or intussusception. Ultrasonography can also detect perforation with ascites and free (peritoneal) air.
RADIATION ENTERITIS — Sonographic changes of radiation enteritis are usually characterized by a slight symmetrical thickening of the intestinal wall. Stenotic intestinal segments may be suggested by hypertrophy of the muscular layer. Bowel wall thickening may be seen in those with radiation colitis, although the finding is nonspecific [259-263].
SARCOIDOSIS — Sarcoidosis of the small bowel, appendix, and the colon is rare [228,264-268]. The most common symptoms are nonbloody diarrhea and abdominal pain. Sonographic signs are nonspecific, showing thickened bowel wall of the small and/or large intestine. Ultrasonography may be helpful for monitoring the therapeutic response.
BOWEL WALL THICKENING DUE TO HEMATOMA — A bowel wall hematoma typically occurs in patients who are coagulopathic. On ultrasonography, the hematoma may be recognized as echo-poor circumscribed bowel wall thickening. A similar picture may be seen in immunoglobulin A vasculitis (IgAV; formerly called Henoch-Schonlein purpura) involving the gastrointestinal tract and with small or large bowel tumors.
SEGMENTAL HYPOECHOIC SMALL BOWEL EDEMA — Segmental hypoechoic small bowel edema is balloon-like hypoechoic swelling of Kerckring's folds that results in a cyst-like appearance. Fluid deposits may be present in Kerckring's folds and in the submucosa. Potential causes of segmental small bowel edema include hereditary angioedema, ACE inhibitor-induced angioedema, vasculitis, mechanical small bowel ileus, gastroenteritis, peritonitis, mesenteric vein thrombosis, small bowel ischemia, mesenteric tumor infiltration, protein deficiency, hyperhydration, and eosinophilic or other granuloma due to anisakiasis [176,269,270]. (See "Miscellaneous nematodes".)
FUNCTIONAL DISORDERS — Ultrasound provides a useful tool for visualization of gastrointestinal motility since it is a real-time imaging methodology in contrast to other imaging methods. However, its role in this setting has not yet been well defined [271,272].
Intragastric maldistribution of a meal in patients with gastroesophageal reflux disease assessed by three-dimensional ultrasonography [273], strain (Doppler) imaging of the stomach [274], and other new modalities are under investigation [60].
RECTAL AND PERINEAL DISORDERS — Perineal ultrasound (PNUS) is an effective, inexpensive, easily available, but still rarely applied diagnostic tool. In addition to demonstration of anatomy, PNUS can be helpful for detecting a variety of pathological conditions of the rectum and perineum, such as transmural inflammation, fistulas, and abscesses in patients with inflammatory bowel disease [5]. PNUS is more flexible than endorectal ultrasound (ERUS), particularly when oblique processes of transsphincteric fistulae are to be examined. For staging of perirectal tumors, PNUS can be used as a complement to conventional ERUS. A valuable extension of the diagnostic application of PNUS is its supportive role during invasive interventions, such as drainage of fluids or targeted puncture of tissue lesions [75,76].
OTHER USES — Positioning of enteral feeding tubes using bedside sonograms may be an alternative to radiologic placement, especially in patients without extensive abdominal surgery [275].
Transabdominal ultrasound, in addition to established endoscopic ultrasound, may help in identifying and characterizing submucosal lesions of the upper and lower gastrointestinal tract, but experience is limited [276].
SUMMARY AND RECOMMENDATIONS
●Background – Transabdominal ultrasonography is most commonly used to obtain images of hepatobiliary, urogenital, and pelvic structures. Improvements in ultrasound technology and increasing familiarity with ultrasonographic findings in a variety of gastrointestinal disorders are broadening its applications for evaluating the small and large intestine. (See 'Introduction' above.)
An advantage of ultrasound imaging compared with endoscopy and contrast radiography is that it permits evaluation of the transmural aspects of inflammatory or neoplastic pathology within its surrounding structures. This can provide an important contribution for diagnosis and monitoring of disease activity. Other advantages are that it is widely available, noninvasive, and can be performed without preparation.
Limitations of ultrasonography are that the alimentary tract cannot be visualized over its entire length, many of the findings are nonspecific, and obtaining and interpreting the images is highly operator-dependent.
●Specific clinical applications – Transabdominal ultrasound can be used to evaluate a number of conditions including:
•Appendicitis (see 'Appendicitis' above)
•Epiploic appendagitis (see 'Epiploic appendagitis' above)
•Diverticulitis (see 'Diverticulitis' above)
•Inflammatory bowel disease (see 'Crohn disease' above and 'Ulcerative colitis' above)
•Infectious enterocolitis (see 'Infectious enterocolitis' above)
•Intussusception (see 'Intussusception' above)
•Tumors (see 'Benign and malignant tumors of the small and large intestine' above)
•Celiac disease (see 'Celiac disease' above)
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