AJR 2004; 183:1285-1291
© American Roentgen Ray Society
Spectrum of Imaging Findings After Intestinal, Liver-Intestinal, or Multivisceral Transplantation: Part 2, Posttransplantation Complications
Karin M. Unsinn1,2,
Alfred Koenigsrainer3,
Michael Rieger2,
Benedikt V. Czermak2,
Helmut Ellemunter1,
Raimund Margreiter3,
Werner R. Jaschke2 and
Martin C. Freund2
1 Department of Pediatrics, Leopold-Franzens University, Anichstrasse 35,
Innsbruck A-6020, Austria.
2 Department of Radiology, Leopold-Franzens University, Innsbruck,
Austria.
3 Department of General Surgery and Transplantation Surgery, Leopold-Franzens
University, Innsbruck, Austria.
Received December 27, 2003;
accepted after revision March 9, 2004.
Address correspondence to K. M. Unsinn.
Introduction
Transplantation of the small bowel, either as isolated intestinal or
combined liver-intestinal or as multivisceral transplantation, has emerged as
a potential alternative to total parenteral nutrition in patients with
irreversible chronic intestinal failure. Compared with other solid organ
transplantations, intestinal transplantation is hampered by the presence of a
large number of immunocompetent donor lymphocytes in gut-associated lymphoid
tissue and mesenteric nodes as well as bacterial contamination, all of which
increase the risk for transplant rejection and infection. In the past decade,
patient and intestinal graft survival rates have improved consistently thanks
to refined surgical techniques, introduction of better immunosuppressive
regimens including tacrolimus, and better antimicrobial therapy of
opportunistic infections. These advances decreased technical and immunologic
failure rates as well as the infection rate. Today transplantation centers
report a 1-year patient and graft survival rate of 81% and 63%, respectively
[1]. However, these rates
compare less favorably with 1-year survival rates associated with solid organs
transplantations of the heart, liver, kidney, and pancreas, which have 1-year
patient and graft survival rates that approach or exceed 90%
[1].
Knowledge of the transplantation procedure and knowledge of postoperative
imaging anatomy of the intestinal graft are basic requirements for
radiologists. Graft survival, among other factors, corresponds to early
diagnosis and therapy for specific graft-related complications including
leakage of enteric anastomosis, abdominal abscess, peritonitis, thrombosis of
graft vessels, hematoma, and posttransplantation lymphoproliferative disorder.
This pictorial essay uses various imaging techniques to show the imaging
spectrum of diseases after isolated intestinal, combined liver-intestinal, or
multivisceral transplantation.
Imaging Techniques
Various imaging techniques are routinely used to detect early or late
posttransplantation complications. During the initial period of intestinal
transplantation in the early 1990s, gastrointestinal studies with barium or
water-soluble contrast material were performed to evaluate the integrity of
the intestinal graft—for example, upper gastrointestinal and small-bowel
series, enteroclysis, and contrast enema
[2,
3]. A Foley catheter blocked
within the isolated intestinal loop after its introduction through the
temporary ileostomy facilitates a retrograde contrast enema examination.
Today, gastrointestinal contrast studies are performed only occasionally to
detect complications of the enteric anastomosis or to evaluate
gastrointestinal motility. Because of the accumulated knowledge of the
clinical pattern of complications, cross-sectional imaging studies are
currently used to detect abnormalities of the vessels, intestinal wall, and
abdominal cavity [4,
5]. The use of sonography and
color-coded sonography to image the vascular system, entire intestinal graft,
and abdominal cavity is hampered by intraluminal intestinal gas
[5], but postoperative motility
of the intestinal graft can be sufficiently evaluated on sonography as a
result of its real-time display. Contrast-enhanced helical CT is the primary
imaging technique for complete evaluation of the vascular and enteric
anastomoses, vessels, intestinal graft, and abdominal cavity
[6]. MRI performed without and
with IV contrast material application may also be useful in evaluating the
intestinal graft, but evaluation of the enteric anastomosis on MRI is
difficult.
Sometimes patients have coexistent impaired renal function before and after
intestinal transplantation; renal function determines the selection of the
appropriate cross-sectional imaging technique. For the preservation of renal
function, contrast-enhanced MRI and unenhanced CT are the preferred
examinations. Catheter angiography is used to confirm vascular complications
while permitting immediate endovascular therapy
[6]. Other imaging-guided
interventions are used to percutaneously treat localized fluid collections,
such as seromas, hematomas, and abscesses.
Imaging techniques are not used to detect transplant rejection or
graft-versus-host disease. Acute rejection is diagnosed by endoscopy and
mucosal biopsies from the donor stomach, duodenum, or distal ileum via the
ileostomy. Graft-versus-host disease manifests most commonly as skin lesions
or mucosal lesions in the recipient's residual gastrointestinal tract; both
sites are best amenable for visual or endoscopic inspection and biopsies.
Imaged Abnormalities
Organ-specific complications after combined liver-intestinal and
multivisceral transplantation concern mainly the intestinal graft and
therefore resemble complications after isolated intestinal transplantation.
These complications rarely involve the hepatic or pancreatic graft because of
the lack of operative manipulation of the hepatobiliary and portal venous
system.
The main complications that are observed after intestinal transplantation
are revealed by imaging techniques: intestinal graft complications including
infection, vascular complications, and other transplantation-associated
complications.
Intestinal Graft Complications Including Infection
Typical graft complications include graft dysmotility, dehiscence,
stricture of the enteric anastomosis, and abdominal infections. Intestinal
graft dysmotility occurs frequently during the early postoperative period and
can be observed directly by real-time sonography or gastrointestinal studies;
it is also suspected on abdominal radiographs and CT scans by the appearance
of a gasless abdomen or increased numbers of air-fluid levels and luminal
dilatation (Fig. 1C).
Anastomotic complications manifest either as dehiscence or stricture and can
involve any anastomosis encountered in intestinal transplantation
procedures.
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Fig. 1C. —41-year-old woman after multivisceral transplantation
necessitated by Gardner's syndrome and intraabdominal desmoid tumor. Eight
months after operation, clinical findings were suggestive of intestinal
obstruction. Helical CT scan obtained without IV but with oral contrast
material shows dilated nonthickened loops of intestinal graft
(asterisks) and air-fluid level, which is consistent with intestinal
dysmotility.
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For the correct interpretation of an imaging study, the radiologist must be
familiar with the presence, location, and type of the various
enteroanastomoses including end-to-end, end-to-side, and side-to-side
reconstruction of intestinal tract continuity. Gastrointestinal contrast
studies are performed with water-soluble contrast material when an anastomotic
dehiscence is suspected. Typically, leakage of contrast material is observed
either contained within or with free communication to the abdominal cavity
(Fig. 2). An anastomotic
stenosis presents as a luminal narrowing on gastrointestinal contrast studies
and may exhibit prestenotic dilatation and dysmotility
(Fig. 1D).
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Fig. 2. —59-year-old man with short-bowel syndrome who underwent upper
gastrointestinal examination with water-soluble contrast material 17 days
after intestinal transplantation using side-to-end jejunojejunal anastomosis.
Image shows contained contrast leakage (open arrow) of recipient
jejunal stump with staple line (solid arrow). Donor jejunum
(solid arrowheads), recipient duodenum (asterisk), and
recipient jejunum (open arrowheads) are also visible.
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Fig. 1D. —41-year-old woman after multivisceral transplantation
necessitated by Gardner's syndrome and intraabdominal desmoid tumor.
Thirty-four months after operation, clinical findings were suggestive of
intestinal obstruction. Radiograph obtained during enema with water-soluble
contrast material displays concentric high-grade stenosis of ileorectal
end-to-side anastomosis (arrow). Air-filled recipient rectal stump
(open arrowheads), contrast-filled distal rectum (asterisk),
and donor ileum (solid arrowheads) are depicted.
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Abdominal infection is a frequent complication after intestinal
transplantation and manifests as abscess (Figs.
3A,
3B,
3C,
3D,
3E,
3F), peritonitis, or fistula
formation. The typical findings for an intraabdominal abscess include a
localized fluid collection with or without gas formation, air-fluid level, and
contrast-enhancing abscess membrane (Fig.
4A). Imaging-guided biopsy is required for definite diagnosis and
for differentiation between abscess and seroma or hematoma. An abscess can
also occur in intraabdominal parenchymal organs; especially the liver is prone
for abscess formation because of its filter function of portal venous drainage
from the intestinal graft (Fig.
4B). The diagnosis of localized or generalized peritonitis is
challenging, even on contrast-enhanced CT or MRI. Imaging findings include
edematous infiltration of the mesenteric fat, increased contrast enhancement
of the intestinal wall, and involved mesenterium
(Fig. 5). Fistula formation
results from an abdominal infection with communication to the skin. Sinus
tract formation involves the retroperitoneum including the psoas muscle.
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Fig. 3A. —3-year-old girl after intestinal transplantation necessitated
by short-bowel syndrome (A-D), graft failure (B-D), and
subsequent retransplantation utilizing multivisceral graft (E and
F). Contrast-enhanced helical CT scan obtained 26 months after initial
intestinal transplantation shows unspecific focal wall thickening of
intestinal graft and reduced contrast enhancement (arrows) compared
with nonthickened regular contrast-enhanced intestinal loops
(arrowheads), which is consistent with focal intestinal ischemia.
Ascites (asterisks) is depicted.
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Fig. 3B. —3-year-old girl after intestinal transplantation necessitated
by short-bowel syndrome (A-D), graft failure (B-D), and
subsequent retransplantation utilizing multivisceral graft (E and
F). Contrast-enhanced MDCT scan obtained 3 years after operation
displays complete acute thrombotic occlusion of portal vein (arrow)
and nonenhancement of spleen (asterisk), indicating infarction.
Gastric tube (arrowhead) is also visible.
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Fig. 3C. —3-year-old girl after intestinal transplantation necessitated
by short-bowel syndrome (A-D), graft failure (B-D), and
subsequent retransplantation utilizing multivisceral graft (E and
F). Contrast-enhanced MDCT scan obtained 3 years after operation also
shows thin-walled pancreatic pseudocyst (solid arrowheads) and focal
ductal dilatation of pancreatic body (single arrow). Ascites
(black asterisk), splenic infarct (white asterisk), and
unspecific focal gastric wall thickening (double arrows) are also
depicted. Open arrowhead = surgical clip.
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Fig. 3D. —3-year-old girl after intestinal transplantation necessitated
by short-bowel syndrome (A-D), graft failure (B-D), and
subsequent retransplantation utilizing multivisceral graft (E and
F). Contrast-enhanced MDCT scan obtained 3 years after operation shows
contrast enhancement of donor superior mesenteric artery (black
arrow) but nonenhancement of graft arteries and intestinal wall
(solid arrowheads), indicating chronic vascular occlusion. Note
additional intraabdominal abscess (open arrowheads) draining via
cutaneous fistula (between white arrows).
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Fig. 3E. —3-year-old girl after intestinal transplantation necessitated
by short-bowel syndrome (A-D), graft failure (B-D), and
subsequent retransplantation utilizing multivisceral graft (E and
F). Contrast-enhanced MDCT scan obtained 3 years after initial
intestinal transplantation with graft failure and 8 weeks after subsequent
multivisceral transplantation with normal graft function shows acute
thrombosis of inferior vena cava (single arrow) at level of renal
veins. Normal enhancement and appearance of intestinal graft (black
asterisks) as well as hyperdense prosthetic mesh inlay (double
arrows) for abdominal wall repair are noted. The following donor anatomic
structures are shown: celiac trunk (single solid arrowhead), duodenum
(white asterisk), pancreas (double open arrowheads),
superior mesenteric artery (double solid arrowheads), and superior
mesenteric vein (single open arrowhead).
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Fig. 3F. —3-year-old girl after intestinal transplantation necessitated
by short-bowel syndrome (A-D), graft failure (B-D), and
subsequent retransplantation utilizing multivisceral graft (E and
F). Contrast-enhanced MDCT scan obtained 3 years after initial
intestinal transplantation with graft failure and 8 weeks after subsequent
multivisceral transplantation with normal graft function displays dissection
membrane (arrow) in abdominal aorta. Asterisks = intestinal graft
loops.
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Fig. 4A. —39-year-old woman after intestinal transplantation
necessitated by Gardner's syndrome with intraabdominal desmoid tumor
(A) and graft failure and subsequent retransplantation utilizing
multivisceral graft (B and C). Contrast-enhanced MDCT scan
obtained 2 months after initial intestinal transplantation displays multiple
intraabdominal abscesses (asterisks) with air-fluid level and
contrast-enhancing abscess membrane. Mesenteric lymphadenopathy (open
arrowhead), partly thickened wall of intestinal graft (solid
arrowhead), and recipient descending colon (double arrows) are
depicted.
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Fig. 4B. —39-year-old woman after intestinal transplantation
necessitated by Gardner's syndrome with intraabdominal desmoid tumor
(A) and graft failure and subsequent retransplantation utilizing
multivisceral graft (B and C). Contrast-enhanced MDCT scan
obtained 2 months after retransplantation that used multivisceral graft
displays multiple intrahepatic focal hypodensities (arrows), which is
consistent with nocardial abscesses. Also, note fluid-filled stomach
(asterisk) and small intraabdominal abscess (arrowhead).
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Fig. 5. —Contrast-enhanced MDCT scan obtained 6 weeks after intestinal
transplantation in 39-year-old man with short-bowel syndrome who presented
with acute sepsis syndrome. Image shows large ventral abdominal wall defect
(between arrows) due to dehiscence and subsequent operative widening
of median laparotomy, intraabdominal abscess (asterisks) with air
bubbles (white arrowheads), and cutaneous drainage (arrows).
Also seen are intestinal graft enlargement due to edematous infiltration,
engorgement of mesenteric vessels, and increased contrast enhancement of
intestinal wall (black arrowheads), all of which are consistent with
surgically proven peritonitis.
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Contrast-enhanced CT sometimes shows an unspecific diffuse thickening of
the intestinal wall and mucosal folds early after transplantation that is
presumably due to edema related to organ procurement and interruption of
draining lymphatic vessels combined with an un-specific enlargement of the
donor's mesenteric lymph nodes (Fig.
6B). CT can also detect an unspecific focal wall thickening of the
small bowel but cannot delineate the underlying cause
(Fig. 3A). Determining the
cause requires additional clinical evaluation or short-term imaging evaluation
and exclusion of rejection or opportunistic infection.
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Fig. 6B. —67-year-old man after multivisceral transplantation
necessitated by liver cirrhosis, intrahepatic hepatocellular carcinoma,
chronic thrombotic occlusion of portomesenteric venous system, and clinical
evidence of infection. Contrast-enhanced helical CT scan obtained 4 weeks
after operation displays unspecific enlargement of mesenteric lymph nodes
(arrows) of intestinal graft. Ascites (asterisks) and
calcification of iliac artery (arrowhead) are also visible.
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Vascular Graft Complications
The most serious vascular complication is arterial and venous graft
thrombosis and can result in intestinal graft necrosis that necessitates graft
enterectomy. Typically, contrast-enhanced CT displays either an intraluminal
filling defect or the complete occlusion of the involved artery and
nonenhancement of the intestinal wall, indicating graft necrosis
(Fig. 3D). Sometimes an
intraluminal membrane can be observed on imaging
(Fig. 3F); this finding is
suggestive of arterial dissection.
In patients with venous thrombosis, contrast-enhanced CT shows an
intraluminal filling defect of the involved vein. Segmental venous thrombosis
of the intestinal graft may result in intestinal pneumatosis
(Fig. 4C). Thrombotic
occlusion of the portal vein is followed by portal hypertension, venous
congestion syndrome, and splenic infarction
(Fig. 3B). Hematomas can also
be detected by various imaging techniques
(Fig. 1A). This finding either
results from clotting disorders or indicates a localized vascular abnormality,
including pseudoaneurysm (Fig.
1A) or vascular anastomotic dehiscence.
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Fig. 4C. —39-year-old woman after intestinal transplantation
necessitated by Gardner's syndrome with intraabdominal desmoid tumor
(A) and graft failure and subsequent retransplantation utilizing
multivisceral graft (B and C). Contrast-enhanced MDCT scan
obtained 3 months after retransplantation that used multivisceral graft shows
nonenhancement of intestinal graft (lower white arrows) except
proximal jejunum (black arrow), focal intramural pneumatosis
(white arrowhead), and free intraabdominal air bubble (black
arrowhead) due to arterial thrombosis with ischemia and perforation.
Localized fluid (white asterisk) with cutaneous fistula (between
upper white arrows) is also depicted.
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Fig. 1A. —41-year-old woman after multivisceral transplantation
necessitated by Gardner's syndrome and intraabdominal desmoid tumor.
Contrast-enhanced helical CT scan obtained 10 days after operation because
laboratory results provided evidence of acute hemorrhage displays mesenteric
pseudoaneurysm (solid black arrowhead) with localized contrast
extravasation (open arrowhead) and mesenteric hematoma (black
asterisk). Intestinal graft lumen (white asterisks), mesenteric
arteries and veins of intestinal graft (arrow), and postoperative
changes in abdominal wall (between white arrowheads) are also
shown.
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Other Transplantation-Associated Complications
Varying degrees of fluid collection are observed after intestinal
transplantation including lymphocele (Fig.
1B) and seroma. Ascites is often located between the intestinal
graft loops. In most patients, these fluid collections regress in size without
treatment, but sometimes percutaneous diagnostic aspiration or therapeutic
drainage is necessary. Posttransplantation lymphoproliferative disorder is a
serious but rare complication of isolated intestinal, multivisceral, and
combined liver-intestinal transplantation that manifests often as involvement
of the intestinal or parenchymal organ graft (Figs.
7A,
7B) or infrequently as
involvement of the recipient's remaining native gastrointestinal tract or as
extraallograft lymphadenopathy
[7]. Complications after
combined liver-intestinal and multivisceral transplantation rarely involve
extraintestinal graft organs but may include fatty liver degeneration
(Fig. 7A), pancreatitis
(Fig. 6A), pancreatic
pseudocyst (Fig. 3C), and
thrombosis of the inferior vena cava (Fig.
3E).
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Fig. 1B. —41-year-old woman after multivisceral transplantation
necessitated by Gardner's syndrome and intraabdominal desmoid tumor. Six weeks
after operation, intestinal graft function was normal. Helical CT scan
obtained after administration of oral and IV contrast material shows large
loculated fluid collection (white asterisk) with displacement of
intestinal graft loops (black asterisks). Subsequent imaging-guided
drainage revealed lymphocele. Postoperative dressing of ileostomy
(arrows) is also depicted.
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Fig. 7A. —5-year-old girl with short-bowel syndrome 4 months after
intestinal transplantation who presented with newly developed ascites.
Arrowhead = gastric tube. Unenhanced MDCT scan shows fatty liver degeneration
(asterisk) and focal hyperdensity (double arrows) in left
liver lobe.
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Fig. 7B. —5-year-old girl with short-bowel syndrome 4 months after
intestinal transplantation who presented with newly developed ascites.
Arrowhead = gastric tube. MDCT scan obtained after contrast enhancement
reveals additional focal intrahepatic hypodensities (single arrows),
which represent pathologically proven multifocal posttransplantation
lymphoproliferative disorder. Contrast-enhancing inferior vena cava
(arrowhead) is also shown. Double arrows = hyperdensity.
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Fig. 6A. —67-year-old man after multivisceral transplantation
necessitated by liver cirrhosis, intrahepatic hepatocellular carcinoma,
chronic thrombotic occlusion of portomesenteric venous system, and clinical
evidence of infection. Contrast-enhanced helical CT scan obtained 2 weeks
after operation shows enlargement of pancreatic head with reduced contrast
enhancement (white arrow), which is consistent with edematous
pancreatitis. Ascites (black asterisks) and periportal lymphedema
(black arrows) are also revealed. Arrowhead = gastric tube, white
asterisk = stomach.
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Introduction
Imaging Techniques
