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Fig. 15. Second stage of small bowel impaired venous there is an indeterminate opacification of some peripheral
drainage. A, B MDCT axial scans show some small bowel branches. C, D Two days later there is progression of the
loops characterized by wall thickness, intramural hemor- impaired venous drainage in the affected loops and an end-
rhage, and submucosal edema; there is no evidence of defi- oluminal defect of filling in the SMV.
nite endoluminal thrombosis in the SMV at the origin, but
b
Fig. 18. Fourth stage of small bowel impaired venous
drainage with infarction. MDCT findings. A Scout view show
evidence of suffering loops in the lower left abdominal quad-
rant. B, C. Axial scans show SMV thrombosis (arrow) and
evidence of markedly thickened small bowel loop, with de-
creased wall enhancement and slight hyperdensity of the
mucosa from hemorrhagic phenomena. Note some intramural
pneumatosis in the segment located in the pelvis. The patient
did not recover after medical therapy and required partial
intestinal resection.
BA (eds). Clinical imaging of the small intestine, 2nd ed. New York:
Springer-Verlag, pp 439–465
pathologic pattern. Radiologic findings correlated with 3. Goldberg MA, Mueller PR, Saini S, et al. (1991) Importance of
clinical symptoms may allow the differentiation of the daily rounds by the radiologist after interventional procedures of
the abdomen and chest. Radiology 180:767–770
ischemic phases and the indication regarding the imme- 4. Scholz FJ (1993) Ischemic bowel disease. Radiol Clin North Am
diate therapy required. 31:1197–1218
5. Sanchez-Fernandez P, Mier y Diaz J, Blanco-Benavides R (2000)
Acute mesenteric ischemia. Profile of an aggresive disease. Rev
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North Am 71:107–124 25. Longo WE, Ballantyne GH, Gusberg RJ (1992) Ischemic colitis:
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Imaging 22:34–41 Saunders, pp 1102–1106
11. Alpern MB, Glazer GM, Francis IR (1988) Ischemic or infarcted 27. Gore RM, Calenoff L, Rogers LF (1979) Roentgenographic man-
bowel: CT findings. Radiology 166:149–152 ifestations of ischemic colitis. JAMA 241:1171–1173
12. Klein HM, Lensing R, Klosterhalfen B, et al. (1995) Diagnostic 28. Greenberg HM, Goldberg HI, Axel L (1981) Colonic ‘‘urticaria’’
imaging of mesenteric infarction. Radiology 197:79–82 pattern due to early ischemia. Gastrointest Radiol 6(2):145–149
13. Federle MP, Chun G, Jeffrey RB, Rayor R (1984) Computed 29. Danse EM, Van Beers BE, Jamart J, et al. (2000) Prognosis of
Tomographic findings in bowel infarction. AJR 142:91–95 ischemic colitis: comparison of color doppler sonography with early
14. Petras RE (2004) Ischemic bowel disease. In: Mills SE (ed). clinical and laboratory findings. AJR 175:1151–1154
Sternberg’s diagnostic surgical pathology. Philadelphia: Lippincott 30. Cheung AH, Jiranek GC, Haggitt RC, et al. (1992) Use of ultra-
Williams & Wilkins, pp 1509–1511 sound to detect intestinal wall ischemia in piglets. Ultrasound Med
15. Grassi R, Di Mizio R, Pinto A, et al. (2004) Serial plain abdominal Biol 18:843–849
film findings in the assessment of acute abdomen: spastic ileus, 31. Cheung AH, Wang KY, Jiranek GC, et al. (1992) Evaluation of a
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108:56–70 bowel ischemia. Invest Radiol 27:217–223
16. Kim JY, Ha HK, Byun JY, et al. (1993) Intestinal infarction sec- 32. Petras RE (2004) Acute ischemic colitis. In: Mills SE (ed). Stern-
ondary to mesenteric venous thrombosis: CT-pathologic correla- berg’s diagnostic surgical pathology. Philadelphia: Lippincott Wil-
tion. JCAT 17:382–385 liams & Wilkins, pp 1495
17. Balthazar EJ, Yen BC, Gordon RB (1999) Ischemic colitis: CT 33. Whitehaed R (1972) The pathology of intestinal ischemia. Clin
evaluation of 54 cases. Radiology 211:381–388 Gastroenterol 1:613–637
18. Robert JH, Mentha G, Rohner A (1993) Ischaemic colitis: two 34. Gore RM, Miller FH, Pereles FS, et al. (2000) Helical CT in the
distinct patterns of severity. Gut 34:4–6 evaluation of the acute abdomen. AJR 174:901–913
19. Marston A, Pheils MT, Thomas ML, Morson BC (1966) Ischaemic 35. Ottinger LW, Austen WG (1967) A study of 136 patients with
colitis. Gut 7:1–15 mesenteric infarction. Surg Gynecol Obstet 124:251–261
20. Brandt LJ, Boley SJ (1993) Ischemic and vascular lesions of the 36. Lund EC, Han SY, Holley HC, et al. (1998) Intestinal ischemia:
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Saunders, pp 1940–1945 37. James S, Balfe DM, Lee JKT, Picus D (1987) Small-bowel disease:
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ª Springer Science+Business Media, Inc. 2005 Abdom Imaging (2005) 30:1–16
Abdominal Published online: DOI: 10.1007/s00261-005-0376-7
Imaging
INVITED UPDATE
Mesenteric ischemia presents as an abdominal emer- neous material and methodology of study. Some
gency due to decreased intestinal blood flow secondary parameters regarding the timing of imaging in which
to mesenteric arterial vascular hypoperfusion, occlu- studies are performed, intravenous and/or oral contrast
sion, or impaired venous drainage [1]. The small bowel medium administration, dynamics of the acute vascular
or colon may be involved. Distinction between intes- injury, and the different etiologies (superior or inferior
tinal ischemia and infarction sometimes is not consid- venous or arterial mesenteric vessels, occlusive or non-
ered adequately in the interpretative process: the occlusive event) are sometimes difficult to summarize in a
ischemia may be a transient and a totally reversible comparative classification. However, diagnostic imaging
event, whereas infarction may be one of the possible may play a pivotal role in the detection of the degree and
consequences that requires surgical or interventional severity of intestinal ischemia and assessment for evi-
management. Despite continuing advances in imaging dence of infarction.
and surgical techniques, early detection of intestinal In the following sections, imaging findings (wall
ischemia before infarction develops remains difficult thickness and enhancement, caliber of intestinal loops,
[2]. Early diagnosis is important to improve survival presence of air-fluid levels, intestinal peristalsis, mesen-
rates [2, 3]; in most cases of late or missed diagnosis, teric arterial and venous vessel viabilities, mural and/or
mortality rate from intestinal infarction is very high, portal/mesenteric pneumatosis) from different method of
from 60% to 90% [4–6]. Prognosis of an ischemic study (abdominal plain film, sonography [US], and
intestinal insult depends upon clinical factors, such as computed tomography [CT]) will be correlated to various
its acuteness, duration and severity, the presence of phases of intestinal changes from ischemia and infarction
collateral vascular circulation, the response of the due to mesenteric vessels hypoperfusion or occlusion
mesenteric vascular branches and intestinal wall to the based on experience in our institutions.
injury [7], extent of intestinal involvement, and the
timeliness of diagnosis and intervention. From a phase Etiology of intestinal ischemia and
in which the intestinal vascular injury may be sus- infarction
pected and the imaging findings of ischemia noted, the Injuries from intestinal ischemia may have an arterial or
severity of mural damage may proceed rapidly to venous origin, with involvement of the superior mesen-
infarction with dire consequences. Differences in bowel teric artery (SMA) or vein (SMV), inferior mesenteric
wall findings may be appreciable between small bowel artery (IMA) or vein (IMV) or from the reduced blood
arterial and venous infarctions [8–10]. flow associated with shunting of blood from the
Radiologic descriptions of intestinal ischemia and splanchnic bed [14]. Extent and site of injury depends
infarction reported in the literature are rich [10–13] but upon anatomic conditions and the presence of collateral
not pathognomonic. Currently, there is no report of a vessels, which often differ across subjects.
direct correlation between bowel wall findings and a
confirmed diagnosis of ischemia or infarction. Most lit-
erature on this topic is characterized by nonhomoge-
Small Bowel, ascending and right transverse
colon
Occlusion of the SMA may be due to embolism or
Correspondence to: S. Romano; email: stefromano@libero.it thrombosis. Emboli may arise from the left atrium in
2 S. Romano et al.: Ischemia and infarction of the small bowel and colon
patients affected by chronic cardiac insufficiency and IMA. Usually observed in the elderly, clinical symp-
fibrillation; however, they may originate from septic tomatology includes left lower abdominal pain and
endocardial foci or from aortic atheromatic plaques. diarrhea; endoscopy may reveal edema and cyanosis of
Emboli may occlude the proximal portion or one of the the sigmoid-rectal mucosa. Leucocytosis is a common
distal branches of the SMA. Occlusive thrombosis in- finding of ischemic disease of the intestine that may
volves more frequently the origin of the SMA, where wall progress to peritonitis with paralytic ileus and shock.
aortic atheroma apposition may cause partial obstruction Impaired venous drainage of the left side of the colon
of the orifice. In case of obstruction of the SMA at the derives from occlusion of the IMV. Thrombophlebitis
origin by an embolus, most of the small intestine and the disease and thrombosis from systemic affections may be
right colon are subject to ischemia. If an atheromatous the underlying cause.
disease progressively occludes the lumen of the vessel, the
formation of collateral vascular circulation may cause a Imaging methods
gradual ischemic insufficiency. Also to be considered is Abdominal plain film remains in most institutions the
the nonocclusive hypoperfusion injury due to a decreased first examination performed in the diagnosis of the acute
systemic arterial supply not related to the presence of abdomen, even in the era of multidetector CT (MDCT)
endoluminal vascular obstruction. technology; the assessment or progression of an intesti-
Although the clinical symptomatology may be vari- nal disease may be followed with this basic imaging
able in case of a nonacute occlusive event, patients with study.
acute SMA occlusion are usually elderly and affected by US may be of interest in follow-up of patients with an
cardiovascular disease, presenting with sudden and se- acute abdomen of indeterminate origin or to monitor a
vere abdominal pain, diarrhea, and vomiting; intestinal pathologic condition that does not require immediate
peristalsis tends to decrease, passing from initial spasm surgery.
to intestinal paralysis. Leucocytosis is usually high and CT examinations using single or multidetector row
there is presence of occult blood in the feces. Patient equipment is performed with intravenous contrast
conditions may rapidly proceed to shock. enhancement; in case of acute abdomen from indetermi-
Alternatively, occlusion of the SMV may be due to nate cause, a delay of 65 sec from the start of injection is
thrombosis originating at the origin or in one of the usually used; however, when the clinical suspicion is
distal branches or from portal thrombosis extending to intestinal infarction, a biphasic study (arterial and venous
mesenteric vessels, causing impaired venous drainage of phases) may be performed. Acquisition of 3-mm slice
the intestinal wall that leads to intramural hemorrhage. thickness may show an optimal intestinal wall evaluation
Frequently observed in patients affected by cirrhosis in most cases. MDCT allows multiplanar reformatting
and/or portal hypertension, mesenteric vein thrombosis with thinner slices, often using specific software proto-
may also be primary. Coagulation disorders such as cols, that may be helpful to study the mesenteric vascular
polycythemia and elevated platelet levels in patients after pattern, especially for the terminal branches. In an
splenectomy, systemic disease such as lupus elythema- emergency, all examinations are performed without
tosis, or the use of estrogen-progesterone therapy may be endoluminal opacification by oral or rectal contrast
related to a risk of developing of mesenteric thrombosis. medium administration in our institutions.
Clinical symptomatology and findings are usually pro-
gressive but similar to those caused by SMA obstruction, Pathophysiology from ischemia to
with abdominal pain, diarrhea, and evidence of occult infarction—imaging findings
blood in the feces. Depending upon the intestinal extent correlations
of the impaired venous drainage, bloody diarrhea, acute
anemia, and hypovolemia may be noted. Small bowel
Arterial etiology
Left transverse, descending, sigmoid colon and Imaging findings related to the pathophysiology of
rectum intestinal vascular injury from arterial occlusion or
The occlusive syndrome of the IMA is uncommon and hypoperfusion may be divided into four stages.
generally due to thrombosis from atherosclerotic disease.
Formation of collateral vessels, from the colic branches First stage. The first and immediate response of the
of the SMA and from the hemorrhoidal arteries, bran- intestine to a vascular injury is spasm of the involved
ches of the hypogastric arteries, are often not effective to loops. Abdominal radiograph at this phase shows a
prevent an acute colorectal ischemia due to occlusion gasless abdomen from spastic ileus (Fig. 1A). US and CT
of the IMA at the origin. In fact, ischemia of the left side examinations may or may not (in case of nonocclusive
of the colon may also be a postoperative complication of hypoperfusion) show an occlusion of the SMA; the bo-
aortic aneurysm surgery that requires sacrifice of the wel wall may show normal enhancement (Fig. 1B).
S. Romano et al.: Ischemia and infarction of the small bowel and colon 3
Fig. 6. Third stage of small bowel ischemia with reperfusion. MDCT (A) coronal and (B) axial views of an SMA thrombosis
(arrow in A); (A, C) note the opacification of the vessel downstream to the occlusion. Some ileal segments appear thickened with
hypodensity of the submucosa (arrow in D) from reperfusion phenomena. Note the renal infarction in B.
the submucosa. Abdominal plain radiograph shows this case may be characterized on plain abdominal film
markedly dilated loops with thickened wall and valvulae by spastic reflex ileus without bowel distention [15] is
conniventes, and diffuse evidence of air-fluid levels difficult to identify. US may show homogeneous hypo-
(Fig. 7A). US shows mainly the presence of extraluminal echoic intestinal wall due to edema that is the earlier
fluid and the absence of peristalsis (Figs. 8, 9). CT change of the submucosa in intestinal infarction [16],
findings may or may not show occlusion of the SMA whereas CT may show a thrombus in the proximal or a
(because persistent hypoperfusion due to luminal nar- peripheral branch of the SMV or into the portal-mes-
rowing without a real thromboembolism may appear enteric vein junction, with homogeneous thickened
with the same findings), bowel wall enhancement is poor intestinal tract involved (Figs. 12, 13).
in case of necrosis, and pneumatosis may be present
(Figs. 10, 11).
Second stage. A subsequent hypotonic reflex ileus on
Venous etiology plain film may be masked by progressive intestinal
Thrombosis of the SMV slows blood flow. The intestinal intramural and mesenteric edema. Intramural blood
vascular injury may be divided into four stages. volume increases as arterial blood keeps flowing into the
bowel wall and the increased intravascular hydrostatic
First stage. Impaired venous drainage disease may pressure dilates the blood vessels, enlarging the fene-
present a less acute symptomatology than arterial strations between the vascular endothelial cells [7]. This
ischemia. Visualization of a true initial phase that also in causes extravasation of plasma, contrast material, or red
6 S. Romano et al.: Ischemia and infarction of the small bowel and colon
blood cells into the bowel wall or lumen; tension in the intestinal wall are preserved; but if the vascular injury
submucosal extravascular compartment or prolonged persists, there are three possibilities: healing, chronicity
stasis-induced thrombosis of the microvessels may cause of the affection, or progression to intestinal infarction.
a stoppage to the arterial flow [7]. Imaging findings at Healing of the affected segment with restitution of ve-
this stage are related to bowel wall thickness, intramural nous flow (Fig. 16) may lead to circumferential granu-
hemorrhage, and submucosal edema. US may show a lation tissue formation in response to the parietal layer
thickened intestinal loop (Fig. 14) with hyperechoic damage.
mucosal layers and hypoechogenicity of the layers due to
edema, and occlusion of the SMV at its origin. SMV
viability may be appreciated at CT examination, yet also Third stage. Persistence of a venous thrombosis leads
in this case the most important CT finding is related to to mesenteric vascular engorgement and edema with
the appearance of the involved intestinal segment, with formation of venous collateral vessels [16]. The imaging
the typical alternating different density layers (‘‘target’’ findings may be commonly observed in patients affected
sign), a more evident hyperdense mucosa due to surface by chronic vascular disorders. Plain radiography may
hemorrhage and ulceration, and a hypodense edematous show a masked intestinal endoluminal air or wall
submucosa (Fig. 15). This stage of impaired venous thickening of some intestinal involved segment. US may
drainage may be reversible because deeper layers of the be used to evaluate the viability of the portal vein and
S. Romano et al.: Ischemia and infarction of the small bowel and colon 7
mesenteric proximal branches and the presence of infarction [17–19]. Pathologic findings of ischemic
thickened bowel wall and peritoneal fluid. CT may re- colitis are mural necrosis and ulceration, submucosal
veal all these findings and mesenteric engorgement edema and hemorrhage, and transmural infarction [17].
(Fig. 17). Ischemic colitis has been considered a form of nonoc-
clusive ischemic disease usually observed in the elderly
[17], without evidence of vascular obstruction of a
Fourth stage. Progression to intestinal infarction causes
major vein or artery and no correlation between the
an extensive submucosal hemorrage and edema. Al-
length and site of colonic involvement and the distri-
though this process seems to be slow, cyanosis may lead
bution of the SMA, SMV, IMA, or IMV [17, 20–22].
to bowel wall loss of integrity, and intestinal bacteria
However, the Griffith and Sudeck points (the junction
may invade the intestinal wall, causing necrosis and
between the distribution of the SMA and IMA near the
peritonitis; serosanguineous or bloody fluid and intia-
splenic flexure and the anastomotic plexus between the
mural and mesenteric vein gas may be appreciated
IMA and the hypogastric supply, respectively) have
Diagnostic findings of infarcted loops due to impaired
been described as most commonly affected by ischemic
venous drainage are marked wall thickness, diffuse mural
colitis [17, 23]. Mucosal damage is usually a self-limited
hypodensity with lack of wall enhancement, and intia-
disease, whereas necrosis of the muscle layer may load
mural and portal-mesenteric pneumatosis. Conventional
to severe stricture, sepsis, or necrosis. Although no
plain film may show the thickened bowel wall and evi-
previous correlation has been established between the
dence of parietal pneumatosis or pneumoperitoneum. US
degree of wall thickening, the length of involvement,
may show a markedly thickened intestinal segment with
and the presence or development of colonic infarction
absence of peristalsis and presence of peritoneal inho-
except for pneumatosis coli [17], a grading scale for
mogeneous fluid. CT findings are related to evidence of
vascular injury to the colon should be done by con-
vascular occlusion, absence of wall enhancement of the
sidering the same morphodynamic changes as for small
intestinal segment involved (Fig. 18), and presence of
bowel from ischemia to infarction. The entire colon
peritoneal fluid and gas in vascular branches, bowel wall,
may be affected, but the distribution may also be
or peritoneum.
patchy and related to the distribution of vascular
branches from superior or inferior mesenteric vessels.
Imaging findings to be considered include site and
Colon length of the colonic affected segment, appearance and
Vascular injury to large bowel comprises a wide spec- degree of wall thickness, pericolic streakiness, presence
trum of pathologic and clinical findings, ranging from of submucosal edema, peritoneal fluid, pneumatosis
an ischemic self-limiting and transient event to bowel coli, mesenteric or portal gas and pneumoperitoneum
8 S. Romano et al.: Ischemia and infarction of the small bowel and colon
Fig. 11. Fourth stage of small bowel ischemia. Coronal sitive contrast medium from previous examinations performed
(A,B) and axial (C) MDCT views of a patient with intestinal in another institution. C Note the diffuse necrosis and intra-
infarction due to occlusion of SMA ileocolic branches mural pneumatosis.
(arrowhead in B). B There is some residual endoluminal po-