Ultrasound Imaging of Bowel Pathology - Technique and Keys To Diagnosis in The Acute Abdomen, 2011

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 OBJECTIVE. This article illustrates the normal and pathologic sonographic appearances
Ashish P. Wasnik1 of bowel, with an emphasis on diagnostic ultrasound techniques.
Aya Kamaya2 CONCLUSION. The current role of ultrasound for adult bowel evaluation is limited in
Jonathan R. Dillman1 the United States, with CT emerging as the primary modality for evaluation of the acute ab-
Ravi K. Kaza1 domen. However, mounting concerns regarding diagnostic radiation and health care costs
may affect practice patterns and shift utilization back toward sonography, which is widely
Amit Pandya1
available and relatively inexpensive.
Rishi K. Maheshwary 1,3
T
Maturen KE, Wasnik AP, Kamaya A, et al. he potential of bowel sonography albeit somewhat nonspecific [7]. Wall thick-
has been recognized for decades ening is more typically concentric in benign
[1, 2]. Although ultrasound re- entities (Fig. 4) and eccentric in malignant
tains an important role for adult entities (Fig. 5), although these categories
bowel evaluation worldwide, its niche in the exhibit considerable overlap [8] (Fig. 6). It
United States is limited. Meanwhile, utiliza- is widely noted that diseased bowel is gen-
tion of CT for evaluation of the acute abdo- erally easier to image with ultrasound than
men continues to increase in this country [3]. normal healthy bowel because motility is of-
The trend is easy to comprehend given the ten decreased and thickened walls are larger
rapid evaluation of bowel and mesentery by and easier to see [8]. A fluid-filled and dis-
Keywords: appendicitis, bowel, inflammatory bowel
CT as well as definitive assessment of ab- tended lumen is also much more amenable to
disease, intussusception, sonography, ultrasound dominal and pelvic organs and major vessels. sonography than a collapsed loop or a loop
Yet, given the massive expansion of medical obscured by gas and its associated artifacts.
DOI:10.2214/AJR.11.6594 radiation exposure [4, 5] and health care
costs [6] in the United States, this practice Normal Mesentery and Omentum
Received January 28, 2011; accepted after revision
May 4, 2011. pattern may prove to be untenable. This ar- Mesenteric and omental fat are generally
ticle seeks to reacquaint radiologists with the inconspicuous except when inflamed. Edema
1
Department of Radiology, University of Michigan gamut of findings in bowel sonography and and infiltration of inflammatory cells tend to
Medical Center, 1500 E Medical Center Dr, B1 D530H, emphasizes specific useful techniques for increase the echogenicity of fat (Figs. 3, 4, 7,
Ann Arbor, MI 48109. Address correspondence to
this imaging modality. and 8). Abnormally echogenic fat may be the
K. E. Maturen (kmaturen@umich.edu).
most conspicuous finding in bowel disease;
2
Department of Radiology, Stanford University Hospitals, Normal “Gut Signature” and this extraluminal finding may indicate an
Stanford, CA. Mural Thickening area of bowel that deserves closer attention
3
From esophagus to rectum, the gastrointes- [8]. “Creeping fat” characteristic of inflam-
Present Address: Department of Radiology, West Penn
Allegheny Health System, Pittsburgh, PA.
tinal tract has a typical multilamellated sono- matory bowel disease, particularly Crohn
graphic appearance, arising from its organized disease, can be striking in both its bulk and
CME and highly stratified histology (Fig. 1). This is echogenicity and may throw relatively hy-
This article is available for CME credit. helpful for at least two reasons: This pattern poechoic reactive mesenteric nodes into high
See www.arrs.org for more information.
allows the sonographer or radiologist to dis- relief [8, 9] (Fig. 8).
WEB tinguish bowel from adjacent structures, and
This is a Web exclusive article. disruption of the pattern aids the diagnosis of Doppler Vascularity
bowel pathology (Figs. 2 and 3). Masses may Color and power Doppler imaging supple-
AJR 2011; 197:W1067–W1075 transgress the layers whereas edema may ex- ment the information provided by gray-scale
0361–803X/11/1976–W1067
pand certain layers or obscure their margins. imaging, with increased vascularity visual-
Bowel-wall thickening may be the most ized in a number of inflammatory and infec-
© American Roentgen Ray Society common and reliable sign of bowel disease, tious diseases in particular (Figs. 2, 8, and 9).
AJR:197, December 2011 W1067

Maturen et al.
Hyperemia, both of bowel wall and adjacent ibility with wall thickness and other imaging plosion of CT utilization. However, many so-
mesentery, is a notable marker of disease ac- features will enable assessment of the signif- nographers and radiologists limit their focus
tivity in inflammatory bowel disease [9–11] icance. However, the efficacy of compression to the solid organs. The pendulum of abdom-
(Fig. 8). Internal vascularity can also enable as a diagnostic indicator may be limited in inal imaging may swing back toward ultra-
distinction between cystic and hypoecho- obese adults. sound. Awareness of normal and pathologic
ic solid structures (Fig. 10). Finally, dimin- sonographic appearances of bowel and atten-
ished vascularity is a specific, although prob- Valsalva Maneuver tion to technique will enable sonographers
ably not sensitive, sign of ischemia [12–14] Hernias of bowel, mesentery, and omen- and radiologists to make optimal use of this
(Figs. 3 and 11). tum may preset as abdominal wall or groin imaging modality because bowel findings
masses, and direct observation while the pa- may be the key element of an otherwise nega-
Dynamic Imaging tient coughs or “bears down” to increase in- tive abdominal ultrasound examination.
Real-time imaging is a unique strength of traabdominal pressure may be quite helpful
ultrasound, although radiologists may inad- (Fig. 17). Such maneuvers may reveal an in- Acknowledgment
vertently forgo this advantage by excessive termittent hernia, show contiguity of a mass We thank Vanessa Allen in Radiology
reliance on the sonographer. Cine clips allow with the intraperitoneal space, allow better Media Services for her help in preparing the
astute sonographers to convey dynamic infor- depiction of the hernia sac or abdominal wall figures for this article.
mation about bowel motility, compressibility, defect, and show reducibility [16, 17]. High-
and changes in position to interpreting radiol- frequency linear transducers (≥ 7 MHz) are References
ogists, but direct observation or performance most appropriate for this evaluation. 1. Jasinski R, Rubin JM, Beezhold C, Aisen A. Ul-
of scanning in problem cases is ideal. trasound examination of the colon. J Clin Ultra-
Focused Scanning sound 1981; 9:206–208
Peristalsis Direct evaluation targeting the area of 2. Fleischer AC, Dowling AD, Weinstein ML, James
Diminished bowel peristalsis is a nonspe- clinical concern may be extremely useful, AE. Sonographic patterns of distended, fluid-
cific indicator of unhealthy small bowel. Re- particularly if the patient is able to local- filled bowel. Radiology 1979; 133:681–685
al-time observation and a sense of the nor- ize the symptoms. A special luxury of ul- 3. Larson DB, Johnson LW, Schnell BM, Salisbury
mal appearance of peristalsis are essential to trasound, focused scanning facilitates de- SR, Forman HP. National trends in CT use in the
making this observation. A variety of causes tection of a variety of bowel and mesenteric emergency department: 1995–2007. Radiology
may impair peristalsis, including high-grade pathologies (Figs. 18 and 19). For superficial 2011; 258:164–173
small-bowel obstruction, ischemia, enteritis, lesions, high-frequency linear transducers 4. Berrington de Gonzalez A, Mahesh M, Kim KP,
and infiltrative processes (Fig. 12). However, may be most appropriate (7–10 MHz), but et al. Projected cancer risks from computed tomo-
it should be noted that hyperperistalsis may their use should be supplemented by lower- graphic scans performed in the United States in
be evident in early or partial small-bowel ob- frequency curved-array imaging (3–8 MHz) 2007. Arch Intern Med 2009; 169:2071–2077
struction. The presence of tethering and ar- to evaluate the complete deep extent of le- 5. Hall EJ, Brenner DJ. Cancer risks from diagnostic
chitectural distortion in association with re- sions. Conversely, when a bowel abnormality radiology. Br J Radiol 2008; 81:362–378
duced peristalsis suggests a more chronic or is initially identified during routine abdom- 6. Centers for Medicare & Medicaid Services Web-
aggressive process, such as transmural in- inal scanning at 3–8 MHz, high-frequency site. National Health Care Expenditures Data.
flammation (as may be seen in Crohn dis- linear transducers can be used secondarily www.cms.gov/NationalHealthCareExpenditures-
ease) or malignancy (Fig. 13). to provide detailed assessment of bowel wall Data2010. Accessed August 17, 2011
and mesentery. Thus, a complete examina- 7. Wilson SR. Gastrointestinal tract sonography.
Compression tion should usually include both probe types. Abdom Imaging 1996; 21:1–8
Healthy bowel can be compressed and 8. Wilson SR. The gastrointestinal tract. In: Rumack
shifted by transducer pressure. Direct pres- Transvaginal Imaging C, Wilson SR, Charbonneau JW, Johnson JM,
sure over an area of abnormality may reveal Transvaginal imaging is a routine part of eds. Diagnostic ultrasound. St Louis, MO: Else-
a lack of normal compressibility in appendi- pelvic imaging in women and may also con- vier Mosby, 2005:269–320
citis (Fig. 14), intussusception (Figs. 11 and tribute to bowel assessment [18, 19]. Deep- 9. Martinez MJ, Ripolles T, Paredes JM, Blanc E,
15), bowel malignancy, or luminal distention ly positioned appendixes may be best visu- Marti-Bonmati L. Assessment of the extension
resulting from obstruction. The graded-com- alized transvaginally (Fig. 14), and other and the inflammatory activity in Crohn’s disease:
pression technique described by Puylaert pathologies, including terminal ileitis, sig- comparison of ultrasound and MRI. Abdom Imag-
[15] enables isolation of abnormal bowel moid or rectal inflammation, and pelvic ing 2009; 34:141–148
loops by pushing away adjacent mobile bow- masses or abscesses (Fig. 20), may be opti- 10. Onali S, Calabrese E, Petruzziello C, et al. Endo-
el. Close approximation of the ultrasound mally assessed in this fashion as well. scopic vs ultrasonographic findings related to
transducer to the area of interest allows use Crohn’s disease recurrence: a prospective longitu-
of higher ultrasound frequencies, yielding Conclusion dinal study at 3 years. J Crohns Colitis 2010;
greater spatial resolution. A cystic or hypo- Given its widespread availability, relative- 4:319–328
echoic mass may be difficult to differentiate ly low cost, and absence of ionizing radiation 11. Spalinger J, Patriquin H, Miron MC, et al. Dop-
from fluid-filled bowel but may be less com- or need for contrast materials, ultrasound has pler US in patients with Crohn disease: vessel
pressible than bowel (Fig. 16) or move sepa- maintained an important role in evaluation of density in the diseased bowel reflects disease ac-
rately from bowel. Correlation of compress- the acute abdomen even during the recent ex- tivity. Radiology 2000; 217:787–791
W1068 AJR:197, December 2011

12. Danse EM, Kartheuser A, Paterson HM, Laterre emic colitis in 58 patients. AJR 2005; 184:777–785 al. Abdominal wall hernias: cross-sectional imag-
PF. Color Doppler sonography of small bowel wall 15. Puylaert JB. Acute appendicitis: US evaluation ing signs of incarceration determined with sonog-
changes in 21 consecutive cases of acute mesen- using graded compression. Radiology 1986; 158: raphy. AJR 2001; 177:1061–1066
teric ischemia. JBR-BTR 2009; 92:202–206 355–360 18. Berton F, Gola G, Wilson S. Perspective on the
13. Danse EM, Van Beers BE, Jamart J, et al. Progno- 16. Jamadar DA, Jacobson JA, Morag Y, et al. Char- role of transrectal and transvaginal sonography of
sis of ischemic colitis: comparison of color Dop- acteristic locations of inguinal region and anterior tumors of the rectum and anal canal. AJR 2008;
pler sonography with early clinical and laboratory abdominal wall hernias: sonographic appearanc- 190:1495–1504
findings. AJR 2000; 175:1151–1154 es and identification of clinical pitfalls. AJR 2007; 19. Chang TS, Bohm-Velez M, Mendelson EB. Non-
14. Ripolles T, Simo L, Martinez-Perez M, Pastor M, 188:1356–1364 gynecologic applications of transvaginal sonogra-
Igual A, Lopez A. Sonographic findings in isch- 17. Rettenbacher T, Hollerweger A, Macheiner P, et phy. AJR 1993; 160:87–93
A B
Fig. 2—52-year-old woman with infectious colitis.
Fig. 1—Images of normal bowel in healthy 36-year-old woman. Gray-scale ultrasound image shows concentric wall
A and B, Transabdominal ultrasound image of upper abdomen (A) shows normal gastric antrum between liver thickening and blurring of normal mural stratification
(liv) and pancreas (panc). Transvaginal image incidentally shows normal rectosigmoid colon (B). Both A and (arrowheads) in colon. Power Doppler image (inset)
B show physiologic lamellation of bowel wall, with five alternating concentric hyperechoic and hypoechoic reveals marked hyperemia (arrow) in affected
bands. Innermost hyperechoic layer (arrowheads) is mucosal surface, followed by hypoechoic muscularis segment.
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.
A B
Fig. 4—6-year-old boy with Crohn disease.
Fig. 3—32-year-old man with perforated, gangrenous appendicitis. Gray-scale ultrasound image shows dramatic
A, Longitudinal gray-scale image through right lower quadrant shows dilated appendix (arrowheads), which is circumferential wall thickening of two adjacent
hypoechoic and relatively featureless with loss of normal mural stratification. small-bowel loops (arrowheads). Note also increased
B, Power Doppler image in same area shows punctuate areas of vascularity adjacent to (arrowheads) but none echogenicity of adjacent mesenteric fat (F),
within appendix. Note also abnormal echogenicity of adjacent inflamed mesenteric fat (arrow). indicating inflammation.

Maturen et al.
A B
Fig. 6—49-year-old man with gastric lymphoma.
Fig. 5—64-year-old woman with locally advanced colon cancer presenting as palpable mass in right upper Transverse gray-scale ultrasound image in left
quadrant. upper quadrant shows markedly thickened and
A, Transverse ultrasound image shows nodular eccentric colonic wall thickening (arrowheads). Contrast this hypoechoic anterior gastric wall (arrowheads) with
with relatively smooth and concentric wall thickening in Figures 2 and 4. loss of lamellation. Posterior wall is obscured by
B, Contrast-enhanced CT image confirms transverse colon mass (arrowheads) with greater nodularity along shadowing from echogenic gas (arrow) in lumen.
anterior mural surface and abdominal wall invasion. 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 Fig. 8—17-year-old girl with Crohn disease. Power Fig. 9—45-year-old man with acute appendicitis.
diverticulitis. Transverse gray-scale image through Doppler image of terminal ileum (arrowheads) shows Noncompressible tubular structure in right lower
left lower quadrant shows wall thickening of sigmoid wall thickening and mural hyperemia, indicating quadrant exhibits marked mural hypervascularity
colon (arrowheads) with associated diverticulum active inflammation. Note also enlarged adjacent (arrowhead) on color Doppler image, solidifying
(calipers). Adjacent mesenteric and omental fat (F) mesenteric lymph node (arrow) surrounded by diagnosis of acute appendicitis.
is abnormally echogenic and attenuating, obscuring echogenic fat.
deeper structures.

A B
Fig. 10—49-year-old man with gastrointestinal
stromal tumor of small bowel. Contrast-enhanced CT Fig. 11—5-month-old girl with massive ileocolic intussusception causing ischemia of distal ileum and right
image shows ovoid soft-tissue mass (arrowheads) hemicolon.
closely associated with distal small bowel. Color A, Gray-scale ultrasound image reveals targetoid noncompressible mass (arrowheads), constituting
Doppler image in same area (inset) had earlier intussusception extending from right lower quadrant to left lower quadrant. Note marked wall thickening and
revealed ovoid well-circumscribed hypoechoic mass loss of stratification, particularly in intussusceptum (outer loop).
with central vascularity (arrowhead). 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.
A B C
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).

Maturen et al.
A B
Fig. 13—24-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.

A B C
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.
A B C
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).

Maturen et al.
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.
A 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 gas-
filled 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.
A B
A B C
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.

Fig. 20—21-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.

Ultrasound Imaging of Bowel Pathology - Technique and Keys To Diagnosis in The Acute Abdomen, 2011

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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

Ultrasound Imaging of Bowel

AJR:197, December 2011 W1067

W1068 AJR:197, December 2011

AJR:197, December 2011 W1069

W1070 AJR:197, December 2011

AJR:197, December 2011 W1071

W1072 AJR:197, December 2011

AJR:197, December 2011 W1073

Fig. 17—57-year-old man with periumbilical hernia.

Fig. 18—37-year-old man with epiploic appendagitis.

W1074 AJR:197, December 2011

Fig. 20—21-year-old woman with pelvic inflammatory disease. Transvaginal

AJR:197, December 2011 W1075

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