G a s t r o i n t e s t i n a l I m a g i n g P i c t o r i a l E s s ay

Maturen et al. Ultrasound Imaging in Acute Abdomen Gastrointestinal Imaging Pictorial Essay

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Ultrasound Imaging of Bowel Pathology: Technique and Keys to Diagnosis in the Acute Abdomen
Katherine E. Maturen1 Ashish P. Wasnik1 Aya Kamaya2 Jonathan R. Dillman1 Ravi K. Kaza1 Amit Pandya1 Rishi K. Maheshwary 1,3
Maturen KE, Wasnik AP, Kamaya A, et al.

OBJECTIVE. This article illustrates the normal and pathologic sonographic appearances of bowel, with an emphasis on diagnostic ultrasound techniques. CONCLUSION. The current role of ultrasound for adult bowel evaluation is limited in the United States, with CT emerging as the primary modality for evaluation of the acute abdomen. However, mounting concerns regarding diagnostic radiation and health care costs may affect practice patterns and shift utilization back toward sonography, which is widely available and relatively inexpensive. he potential of bowel sonography has been recognized for decades [1, 2]. Although ultrasound retains an important role for adult bowel evaluation worldwide, its niche in the United States is limited. Meanwhile, utilization of CT for evaluation of the acute abdomen continues to increase in this country [3]. The trend is easy to comprehend given the rapid evaluation of bowel and mesentery by CT as well as definitive assessment of abdominal and pelvic organs and major vessels. Yet, given the massive expansion of medical radiation exposure [4, 5] and health care costs [6] in the United States, this practice pattern may prove to be untenable. This article seeks to reacquaint radiologists with the gamut of findings in bowel sonography and emphasizes specific useful techniques for this imaging modality. Normal Gut Signature and Mural Thickening From esophagus to rectum, the gastrointestinal tract has a typical multilamellated sonographic appearance, arising from its organized and highly stratified histology (Fig. 1). This is helpful for at least two reasons: This pattern allows the sonographer or radiologist to distinguish bowel from adjacent structures, and disruption of the pattern aids the diagnosis of bowel pathology (Figs. 2 and 3). Masses may transgress the layers whereas edema may expand certain layers or obscure their margins. Bowel-wall thickening may be the most common and reliable sign of bowel disease,

Keywords: appendicitis, bowel, inflammatory bowel disease, intussusception, sonography, ultrasound DOI:10.2214/AJR.11.6594 Received January 28, 2011; accepted after revision May 4, 2011.
1 Department of Radiology, University of Michigan Medical Center, 1500 E Medical Center Dr, B1 D530H, Ann Arbor, MI 48109. Address correspondence to K.E.Maturen (kmaturen@umich.edu). 2 Department of Radiology, Stanford University Hospitals, Stanford, CA. 3

albeit somewhat nonspecific [7]. Wall thickening is more typically concentric in benign entities (Fig. 4) and eccentric in malignant entities (Fig. 5), although these categories exhibit considerable overlap [8] (Fig. 6). It is widely noted that diseased bowel is generally easier to image with ultrasound than normal healthy bowel because motility is often decreased and thickened walls are larger and easier to see [8]. A fluid-filled and distended lumen is also much more amenable to sonography than a collapsed loop or a loop obscured by gas and its associated artifacts. Normal Mesentery and Omentum Mesenteric and omental fat are generally inconspicuous except when inflamed. Edema and infiltration of inflammatory cells tend to increase the echogenicity of fat (Figs. 3, 4, 7, and 8). Abnormally echogenic fat may be the most conspicuous finding in bowel disease; this extraluminal finding may indicate an area of bowel that deserves closer attention [8]. Creeping fat characteristic of inflammatory bowel disease, particularly Crohn disease, can be striking in both its bulk and echogenicity and may throw relatively hypoechoic reactive mesenteric nodes into high relief [8, 9] (Fig. 8). Doppler Vascularity Color and power Doppler imaging supplement the information provided by gray-scale imaging, with increased vascularity visualized in a number of inflammatory and infectious diseases in particular (Figs. 2, 8, and 9).

Present Address: Department of Radiology, West Penn Allegheny Health System, Pittsburgh, PA.

CME This article is available for CME credit. See www.arrs.org for more information. WEB This is a Web exclusive article. AJR 2011; 197:W1067W1075 0361803X/11/1976W1067 American Roentgen Ray Society

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Maturen et al. Hyperemia, both of bowel wall and adjacent mesentery, is a notable marker of disease activity in inflammatory bowel disease [911] (Fig. 8). Internal vascularity can also enable distinction between cystic and hypoechoic solid structures (Fig. 10). Finally, diminished vascularity is a specific, although probably not sensitive, sign of ischemia [1214] (Figs. 3 and 11). Dynamic Imaging Real-time imaging is a unique strength of ultrasound, although radiologists may inadvertently forgo this advantage by excessive reliance on the sonographer. Cine clips allow astute sonographers to convey dynamic information about bowel motility, compressibility, and changes in position to interpreting radiologists, but direct observation or performance of scanning in problem cases is ideal. Peristalsis Diminished bowel peristalsis is a nonspecific indicator of unhealthy small bowel. Real-time observation and a sense of the normal appearance of peristalsis are essential to making this observation. A variety of causes may impair peristalsis, including high-grade small-bowel obstruction, ischemia, enteritis, and infiltrative processes (Fig. 12). However, it should be noted that hyperperistalsis may be evident in early or partial small-bowel obstruction. The presence of tethering and architectural distortion in association with reduced peristalsis suggests a more chronic or aggressive process, such as transmural inflammation (as may be seen in Crohn disease) or malignancy (Fig. 13). Compression Healthy bowel can be compressed and shifted by transducer pressure. Direct pressure over an area of abnormality may reveal a lack of normal compressibility in appendicitis (Fig. 14), intussusception (Figs. 11 and 15), bowel malignancy, or luminal distention resulting from obstruction. The graded-compression technique described by Puylaert [15] enables isolation of abnormal bowel loops by pushing away adjacent mobile bowel. Close approximation of the ultrasound transducer to the area of interest allows use of higher ultrasound frequencies, yielding greater spatial resolution. A cystic or hypoechoic mass may be difficult to differentiate from fluid- filled bowel but may be less compressible than bowel (Fig. 16) or move separately from bowel. Correlation of compressibility with wall thickness and other imaging features will enable assessment of the significance. However, the efficacy of compression as a diagnostic indicator may be limited in obese adults. Valsalva Maneuver Hernias of bowel, mesentery, and omentum may preset as abdominal wall or groin masses, and direct observation while the patient coughs or bears down to increase intraabdominal pressure may be quite helpful (Fig. 17). Such maneuvers may reveal an intermittent hernia, show contiguity of a mass with the intraperitoneal space, allow better depiction of the hernia sac or abdominal wall defect, and show reducibility [16, 17]. Highfrequency linear transducers ( 7 MHz) are most appropriate for this evaluation. Focused Scanning Direct evaluation targeting the area of clinical concern may be extremely useful, particularly if the patient is able to localize the symptoms. A special luxury of ultrasound, focused scanning facilitates detection of a variety of bowel and mesenteric pathologies (Figs. 18 and 19). For superficial lesions, high-frequency linear transducers may be most appropriate (710 MHz), but their use should be supplemented by lowerfrequency curved-array imaging (38 MHz) to evaluate the complete deep extent of lesions. Conversely, when a bowel abnormality is initially identified during routine abdominal scanning at 38 MHz, high-frequency linear transducers can be used secondarily to provide detailed assessment of bowel wall and mesentery. Thus, a complete examination should usually include both probe types. Transvaginal Imaging Transvaginal imaging is a routine part of pelvic imaging in women and may also contribute to bowel assessment [18, 19]. Deeply positioned appendixes may be best visualized transvaginally (Fig. 14), and other pathologies, including terminal ileitis, sigmoid or rectal inflammation, and pelvic masses or abscesses (Fig. 20), may be optimally assessed in this fashion as well. Conclusion Given its widespread availability, relatively low cost, and absence of ionizing radiation or need for contrast materials, ultrasound has maintained an important role in evaluation of the acute abdomen even during the recent explosion of CT utilization. However, many sonographers and radiologists limit their focus to the solid organs. The pendulum of abdominal imaging may swing back toward ultrasound. Awareness of normal and pathologic sonographic appearances of bowel and attention to technique will enable sonographers and radiologists to make optimal use of this imaging modality because bowel findings may be the key element of an otherwise negative abdominal ultrasound examination. Acknowledgment We thank Vanessa Allen in Radiology Media Services for her help in preparing the figures for this article. References
1. Jasinski R, Rubin JM, Beezhold C, Aisen A. Ultrasound examination of the colon. J Clin Ultrasound 1981; 9:206208 2. Fleischer AC, Dowling AD, Weinstein ML, James AE. Sonographic patterns of distended, fluidfilled bowel. Radiology 1979; 133:681685 3. Larson DB, Johnson LW, Schnell BM, Salisbury SR, Forman HP. National trends in CT use in the emergency department: 19952007. Radiology 2011; 258:164173 4. Berrington de Gonzalez A, Mahesh M, Kim KP, et al. Projected cancer risks from computed tomographic scans performed in the United States in 2007. Arch Intern Med 2009; 169:20712077 5. Hall EJ, Brenner DJ. Cancer risks from diagnostic radiology. Br J Radiol 2008; 81:362378 6. Centers for Medicare & Medicaid Services Website. National Health Care Expenditures Data. www.cms.gov/NationalHealthCareExpendituresData2010. Accessed August 17, 2011 7. Wilson SR. Gastrointestinal tract sonography. Abdom Imaging 1996; 21:18 8. Wilson SR. The gastrointestinal tract. In: Rumack C, Wilson SR, Charbonneau JW, Johnson JM, eds. Diagnostic ultrasound. St Louis, MO: Elsevier Mosby, 2005:269320 9. Martinez MJ, Ripolles T, Paredes JM, Blanc E, Marti-Bonmati L. Assessment of the extension and the inflammatory activity in Crohns disease: comparison of ultrasound and MRI. Abdom Imaging 2009; 34:141148 10. Onali S, Calabrese E, Petruzziello C, et al. Endoscopic vs ultrasonographic findings related to Crohns disease recurrence: a prospective longitudinal study at 3 years. J Crohns Colitis 2010; 4:319328 11. Spalinger J, Patriquin H, Miron MC, et al. Doppler US in patients with Crohn disease: vessel density in the diseased bowel reflects disease activity. Radiology 2000; 217:787791

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12. Danse EM, Kartheuser A, Paterson HM, Laterre PF. Color Doppler sonography of small bowel wall changes in 21 consecutive cases of acute mesenteric ischemia. JBR-BTR 2009; 92:202206 13. Danse EM, Van Beers BE, Jamart J, et al. Prognosis of ischemic colitis: comparison of color Doppler sonography with early clinical and laboratory findings. AJR 2000; 175:11511154 14. Ripolles T, Simo L, Martinez-Perez M, Pastor M, Igual A, Lopez A. Sonographic findings in ischemic colitis in 58 patients. AJR 2005; 184:777785 15. Puylaert JB. Acute appendicitis: US evaluation using graded compression. Radiology 1986; 158: 355360 16. Jamadar DA, Jacobson JA, Morag Y, et al. Characteristic locations of inguinal region and anterior abdominal wall hernias: sonographic appearances and identification of clinical pitfalls. AJR 2007; 188:13561364 17. Rettenbacher T, Hollerweger A, Macheiner P, et al. Abdominal wall hernias: cross-sectional imaging signs of incarceration determined with sonography. AJR 2001; 177:10611066 18. Berton F, Gola G, Wilson S. Perspective on the role of transrectal and transvaginal sonography of tumors of the rectum and anal canal. AJR 2008; 190:14951504 19. Chang TS, Bohm-Velez M, Mendelson EB. Nongynecologic applications of transvaginal sonography. AJR 1993; 160:8793

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Fig. 1 Images of normal bowel in healthy 36-year-old woman. A and B, Transabdominal ultrasound image of upper abdomen ( A ) shows normal gastric antrum between liver (liv) and pancreas (panc). Transvaginal image incidentally shows normal rectosigmoid colon (B). Both A and B show physiologic lamellation of bowel wall, with five alternating concentric hyperechoic and hypoechoic bands. Innermost hyperechoic layer (arrowheads ) is mucosal surface, followed by hypoechoic muscularis mucosa, hyperechoic submucosa, hypoechoic muscularis propria, and outermost hyperechoic serosal surface (arrows ). Muscle is usually hypoechoic and fat is usually hyperechoic, but disease states can alter these normal appearances.

Fig. 2 52-year-old woman with infectious colitis. Gray-scale ultrasound image shows concentric wall thickening and blurring of normal mural stratification (arrowheads ) in colon. Power Doppler image (inset ) reveals marked hyperemia (arrow ) in affected segment.

Fig. 3 32-year-old man with perforated, gangrenous appendicitis. A, Longitudinal gray-scale image through right lower quadrant shows dilated appendix (arrowheads ), which is hypoechoic and relatively featureless with loss of normal mural stratification. B, Power Doppler image in same area shows punctuate areas of vascularity adjacent to (arrowheads ) but none within appendix. Note also abnormal echogenicity of adjacent inflamed mesenteric fat (arrow ).

Fig. 4 6-year-old boy with Crohn disease. Gray-scale ultrasound image shows dramatic circumferential wall thickening of two adjacent small-bowel loops (arrowheads ). Note also increased echogenicity of adjacent mesenteric fat (F), indicating inflammation.

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A
Fig. 5 64-year-old woman with locally advanced colon cancer presenting as palpable mass in right upper quadrant. A, Transverse ultrasound image shows nodular eccentric colonic wall thickening (arrowheads ). Contrast this with relatively smooth and concentric wall thickening in Figures 2 and 4. B, Contrast-enhanced CT image confirms transverse colon mass (arrowheads ) with greater nodularity along anterior mural surface and abdominal wall invasion.

Fig. 6 49-year-old man with gastric lymphoma. Transverse gray-scale ultrasound image in left upper quadrant shows markedly thickened and hypoechoic anterior gastric wall (arrowheads ) with loss of lamellation. Posterior wall is obscured by shadowing from echogenic gas (arrow ) in lumen. Contrast-enhanced CT image (inset ) confirms marked circumferential wall thickening of stomach (arrowheads ) resulting from lymphomatous mural infiltration.

Fig. 7 56-year-old man with acute sigmoid diverticulitis. Transverse gray-scale image through left lower quadrant shows wall thickening of sigmoid colon (arrowheads ) with associated diverticulum (calipers ). Adjacent mesenteric and omental fat (F) is abnormally echogenic and attenuating, obscuring deeper structures.

Fig. 817-year-old girl with Crohn disease. Power Doppler image of terminal ileum (arrowheads ) shows wall thickening and mural hyperemia, indicating active inflammation. Note also enlarged adjacent mesenteric lymph node (arrow ) surrounded by echogenic fat.

Fig. 9 45-year-old man with acute appendicitis. Noncompressible tubular structure in right lower quadrant exhibits marked mural hypervascularity (arrowhead ) on color Doppler image, solidifying diagnosis of acute appendicitis.

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Fig. 10 49-year-old man with gastrointestinal stromal tumor of small bowel. Contrast-enhanced CT image shows ovoid soft-tissue mass (arrowheads ) closely associated with distal small bowel. Color Doppler image in same area (inset ) had earlier revealed ovoid well-circumscribed hypoechoic mass with central vascularity (arrowhead ).

Fig. 11 5-month-old girl with massive ileocolic intussusception causing ischemia of distal ileum and right hemicolon. A, Gray-scale ultrasound image reveals targetoid noncompressible mass (arrowheads ), constituting intussusception extending from right lower quadrant to left lower quadrant. Note marked wall thickening and loss of stratification, particularly in intussusceptum (outer loop). B, Color Doppler image shows some vascularity (arrowheads ) in tissue surrounding mass but none within loops of intussusceptum. Punctuate and linear echogenic mural foci (arrows ) are areas of pneumatosis.

Fig. 12 60-year-old man with graft-versus-host disease of small bowel and colon after unrelated donor bone marrow transplantation for B cell acute lymphoblastic leukemia. A, Gray-scale ultrasound image of left upper quadrant shows multiple aperistaltic small and large bowel loops, some with echogenic thickened walls (arrowheads ). B, Longitudinal ultrasound image through same area as A shows circumferential wall thickening of descending colon (arrowhead ), with abnormal echogenicity and loss of normal gut signature. C, Unenhanced CT image confirms diffusely dilated and featureless small and large bowel (arrowhead ).

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Fig. 1324-year-old woman with gastric carcinoma and peritoneal carcinomatosis. A, Gray-scale ultrasound image of left upper quadrant shows matted, thick-walled small-bowel loops (arrowhead ) adjacent to spleen (S). Minimal peristalsis could be seen in real time. Contrast-enhanced CT image (inset ) confirms peritoneal carcinomatosis with serosal implants tethering dilated small bowel (arrow ). B, Transabdominal ultrasound image through pelvis reveals complex cystic mass (M) with mural nodules (arrowheads). Contrast-enhanced CT image (inset ) also illustrates mixed cystic and solid pelvic metastasis (star ).

Fig. 14 51-year-old woman with early acute appendicitis. Transvaginal ultrasound images with (left ) and without (right ) compression show no change in diameter of dilated appendix (arrowheads ). Note preservation of normal gut wall stratification in contrast to Figure 3.

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Fig. 15 84-year-old woman with ileocolic intussusception resulting from cecal adenocarcinoma. A, Gray-scale ultrasound image through right lower quadrant shows large noncompressible tubular mass (arrowheads ). B, Color Doppler image shows multiple small linear vessels (arrowheads ) within mass. Core of mass is largely hyperechoic with striated appearance. This reflects presence of bowel, mesenteric fat, and vessels within intussusception. C, Contrast-enhanced CT image confirms ileocolic intussusceptum (arrowheads ) containing bowel with accompanying mesenteric fat and enhancing vessels. Intussusception in adults nearly always indicates underlying mass; lead point was colon cancer (not shown), confirmed at surgery in this patient.

Fig. 16 52-year-old woman with appendiceal mucocele. A, Color Doppler ultrasound image in right lower quadrant shows noncompressible complex cystic mass (arrowheads ) containing thin septations (arrow ) and no significant internal vascularity. B, Contrast-enhanced CT image confirms cystic mass (arrowheads ) closely associated with cecum (arrow ). C, Septae and fine calcifications (arrows ) within mass favor mucinous histology. Pathology confirmed benign appendiceal mucocele (mucinous cystadenoma of appendix).

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Fig. 17 57-year-old man with periumbilical hernia. A, Transverse midline ultrasound image shows tubular structure (arrowheads ) protruding toward skin surface just medial to rectus muscle (R). B, Ultrasound image shows bulge changes and enlarges (arrowheads ) with Valsalva maneuver, compatible with hernia. Some peristalsis was appreciable in real time, confirming bowel content in hernia sac.

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B
Fig. 18 37-year-old man with epiploic appendagitis. A, Gray-scale ultrasound image in area of pain shows ovoid well-circumscribed echogenic nodule with hypoechoic rim (arrowheads ). This lesion was round in both dimensions, not tubular, and adjacent to gasfilled colon. B, Contrast-enhanced CT image in same area shows focus of encapsulated fat (arrowheads ) along antimesenteric side of right hemicolon. There is mild adjacent inflammatory change.

Fig. 19 6-year-old boy with Meckel diverticulitis. A, Transverse gray-scale ultrasound image in area of pain revealed thick-walled fluid-filled structure with gut signature (arrowheads ) just deep in relation to abdominal wall. B, Longitudinal image through same area confirms ovoid shape of this lesion (arrowheads ) and its contiguity with adjacent bowel (arrows ). C, Contrast-enhanced CT image shows thick-walled bowel diverticulum (arrowheads ) with adjacent inflammation. A Meckel diverticulum with focal perforation at base was found at laparoscopy.

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Fig. 2021-year-old woman with pelvic inflammatory disease. Transvaginal ultrasound image shows complex fluid compatible with pus (P) surrounding uterus (Ut). Adjacent small-bowel loop is dilated and thick-walled (arrowheads ), reflecting reactive enteritis and ileus. Note also increased echogenicity of pelvic and mesenteric fat (arrows ), further indicator of inflammation.

F O R YO U R I N F O R M AT I O N

This article is available for CME credit. See www.arrs.org for more information.

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