DOI:10.2214/AJR.06.1046
AJR 2007; 189:89-99
© American Roentgen Ray Society
Cystic Fibrosis in Children and Young Adults: Findings on Routine Abdominal Sonography
Hans P. Haber1
1 Department of Pediatrics, University of Tuebingen, Hoppe-Seyler-Str. 1,
D-72076 Tuebingen, Germany.
Received August 8, 2006;
accepted after revision January 15, 2007.
Address correspondence to H. P. Haber
(peter.haber{at}med.uni-tuebingen.de).
Abstract
OBJECTIVE. The gastrointestinal manifestations of cystic fibrosis
predispose patients to morbid conditions involving the pancreas, liver,
biliary tract, spleen, and intestine. This article reviews the sonographic
appearance of these abdominal manifestations.
CONCLUSION. Numerous gastrointestinal complications have sonographic
manifestations that must be interpreted correctly to ensure appropriate
therapy.
Keywords: cystic fibrosis • liver disease • pancreaticobiliary imaging • pediatric imaging • small bowel • sonography
Introduction
Cystic fibrosis (CF) is the most common lethal genetic defect in white
populations [1]. Biochemical
studies have shown dysfunction of epithelial chloride transport caused by
defects in the CF transmembrane regulation (CFTR) gene on chromosome
7. The dysfunction produces abnormally thick secretions that cause abnormal
changes throughout multiple organ systems, such as the lungs, pancreas, liver,
intestine, and reproductive tract. Gastrointestinal symptoms occur in
85–90% of cases of CF
[1–3].
Because of diagnostic and therapeutic advances, life expectancy has
lengthened. A larger number of older children and young adults than in the
past are at risk of abdominal complications such as fecal impaction,
appendicitis, intussusception, fibrosing colonopathy, liver cirrhosis, and
portal hypertension [2].
Abdominal sonography, used commonly in the diagnostic evaluation, can depict
abnormalities of the pancreas, liver, gallbladder, spleen, and bowel.
Awareness of these manifestations is important not only in evaluation of the
extent of disease but also in determining treatment requirements and efficacy
in patients with CF.
This article reviews the sonographic appearance of the abdominal
manifestations of CF. One hundred twenty patients with CF whose ages ranged
from 1 month to 27 years underwent routine abdominal sonography over 8 years.
The examinations were part of the usual protocol for evaluation of CF
performed to detect liver disease and to monitor bowel-wall thickening during
follow-up. The sonographic system used (Sonoline Elegra or Antares, Siemens
Medical Solutions) had 7.5-MHz curved array and high-resolution 12-MHz linear
array probes.
Pancreas
By childhood, approximately 85% of CF patients have pancreatic exocrine
insufficiency, which causes steatorrhea, flatulence, and abdominal pain
[3,
4]. The pancreatic lesions are
caused by obstruction of small ducts by secretions and cellular debris. The
abnormal changes in the pancreas are a function of the duration and intensity
of CF [3]. On sonography, the
severely affected pancreas is hyperechoic and small, signs of the presence of
pancreatic atrophy and replacement of the pancreatic parenchyma by fibrous
tissue and fat [4,
5] (Figs.
1A,
1B,
2A, and
2B). Hypoechoic areas
representing pancreatic fibrosis sometimes are found, as are pancreatic
calcifications and small pancreatic cysts measuring 1–3 mm (Figs.
3A and
3B). Pancreatic cystosis,
complete replacement of the pancreas by cysts, is well depicted with
sonography, CT, and MRI [6]
(Figs. 4A and
4B). Pancreatitis is a rare
complication among patients with CF. The reported incidence was 1.2% in a
large cohort of patients with CF
[7]. Pancreatitis should be
considered in all patients with suggestive clinical features.
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Fig. 1A —9-year-old boy with cystic fibrosis and pancreatic exocrine
insufficiency. Longitudinal (A) and transverse (B) sonograms at
level of pancreatic head show small pancreas (arrows) with areas of
markedly increased echogenicity, resembling echogenicity of retroperitoneal
fat (star, A). Scale segment distance, 10 mm. s = superior
mesenteric artery, ao = aorta.
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Fig. 1B —9-year-old boy with cystic fibrosis and pancreatic exocrine
insufficiency. Longitudinal (A) and transverse (B) sonograms at
level of pancreatic head show small pancreas (arrows) with areas of
markedly increased echogenicity, resembling echogenicity of retroperitoneal
fat (star, A). Scale segment distance, 10 mm. s = superior
mesenteric artery, ao = aorta.
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Fig. 2A —9-year-old boy in good health. Longitudinal (A) and
transverse (B) sonograms show normal pancreas (arrows) for
comparison with Figures 1A and
1B. Pancreatic echogenicity is
equivalent to that of liver. Scale segment distance, 10 mm. Star indicates
retroperitoneal fat. ao = aorta, vci = inferior vena cava.
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Fig. 2B —9-year-old boy in good health. Longitudinal (A) and
transverse (B) sonograms show normal pancreas (arrows) for
comparison with Figures 1A and
1B. Pancreatic echogenicity is
equivalent to that of liver. Scale segment distance, 10 mm. Star indicates
retroperitoneal fat. ao = aorta, vci = inferior vena cava.
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Fig. 3A —37-year-old man with asymptomatic cystic fibrosis and
pancreatic fibrosis. ao = aorta, s = superior mesenteric artery, vci =
inferior vena cava. Transverse sonogram at level of pancreatic head
(arrow) shows hypoechoic areas representing areas of fibrosis. Small
anechoic areas within pancreas represent small cysts. Tiny echogenic foci with
acoustic shadowing represent pancreatic calcification. Scale segment distance,
5 mm.
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Fig. 3B —37-year-old man with asymptomatic cystic fibrosis and
pancreatic fibrosis. ao = aorta, s = superior mesenteric artery, vci =
inferior vena cava. Axial contrast-enhanced T1-weighted MR image obtained at
same level as A shows intermixed low signal intensity (arrow)
representing pancreatic fibrosis.
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Fig. 4A —12-year-old boy with asymptomatic cystic fibrosis and
pancreatic cystosis. Longitudinal (A) and transverse (B)
sonograms at level of pancreatic head show enlarged pancreas with numerous
sonolucent lesions (arrows) corresponding to cysts distributed
throughout gland. Small amount of echogenic pancreatic tissue is present
between cysts. Scale segment distance, 10 mm. ao = aorta.
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Fig. 4B —12-year-old boy with asymptomatic cystic fibrosis and
pancreatic cystosis. Longitudinal (A) and transverse (B)
sonograms at level of pancreatic head show enlarged pancreas with numerous
sonolucent lesions (arrows) corresponding to cysts distributed
throughout gland. Small amount of echogenic pancreatic tissue is present
between cysts. Scale segment distance, 10 mm. ao = aorta.
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Liver
Hepatic involvement in CF is common. It ranges from hepatic steatosis to
characteristic focal biliary fibrosis and eventual multilobular biliary
cirrhosis. Studies have shown an increasing incidence of liver involvement
with age, ranging from 20% to 50%. However, only approximately 1–5% of
cases progress to clinically apparent liver disease
[2]. Steatosis of the liver is
not rare in neonates and infants
[4]. Hepatic enlargement and
enhanced echogenicity representing fatty infiltration of the liver are the
classic sonographic findings (Figs.
5A,
5B, and
5C). There is no evidence to
suggest that steatosis progresses to cirrhosis
[2].
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Fig. 5A —5-year-old girl with cystic fibrosis, hepatic steatosis, and
slightly elevated liver enzyme levels. Scale segment distance, 10 mm.
Longitudinal (A) and transverse (B) sonograms (3.5-MHz probe) of
right lobe of liver show coarse liver parenchyma with diffusely enhanced
echogenicity. In comparison, kidney (star) appears hypoechoic.
Diminished through-transmission is evident.
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Fig. 5B —5-year-old girl with cystic fibrosis, hepatic steatosis, and
slightly elevated liver enzyme levels. Scale segment distance, 10 mm.
Longitudinal (A) and transverse (B) sonograms (3.5-MHz probe) of
right lobe of liver show coarse liver parenchyma with diffusely enhanced
echogenicity. In comparison, kidney (star) appears hypoechoic.
Diminished through-transmission is evident.
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Fig. 5C —5-year-old girl with cystic fibrosis, hepatic steatosis, and
slightly elevated liver enzyme levels. Scale segment distance, 10 mm.
High-resolution sonogram through right lobe of liver shows poor visualization
of portal triads (arrows).
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Focal biliary fibrosis, characterized by eosinophilic concretions and
variable portal fibrosis, is pathognomonic of CF-related liver disease and
affects more than 20% of children and adolescents with CF. On sonography, the
liver exhibits hyperechoic periportal thickening caused by fibrosis or focal
fat. Diffuse increased echogenicity of the liver parenchyma also is present
(Figs. 6A and
6B). The sonographic findings
may precede clinical and biochemical evidence of liver disease.
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Fig. 6A —15-year-old girl with asymptomatic cystic fibrosis and focal
biliary fibrosis. Longitudinal sonogram of left lobe shows coarse
heterogeneous hepatic parenchyma and diminished visibility of intrahepatic
vessels. Scale segment distance, 10 mm.
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Fig. 6B —15-year-old girl with asymptomatic cystic fibrosis and focal
biliary fibrosis. High-resolution sonogram of liver shows irregular
echotexture and hyperechoic periportal thickening (arrows) due to
presence of focal fat.
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Approximately 5% of cases of focal biliary fibrosis progress to
multilobular biliary cirrhosis characterized by irregular regeneration nodules
larger than those usually seen in other forms of biliary or portal cirrhosis
and with extensive fibrosis and bile duct proliferation. Jaundice is rare, and
in many instances, results of liver function tests are unremarkable
[3]. Sonography reveals a
small, nodular liver with irregular echotexture (Figs.
7A and
7B). When portal hypertension
develops, splenic enlargement, portosystemic collateral vessels, and,
occasionally, ascites are seen on sonography
[4] (Figs.
8A,
8B,
8C, and
8D).
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Fig. 7A —21-year-old man with cystic fibrosis, multilobular biliary
cirrhosis, and slightly elevated liver enzyme levels. Longitudinal sonogram of
left lobe of liver shows small heterogeneous liver with numerous large,
irregular regenerative nodules (stars). Scale segment distance, 10
mm.
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Fig. 7B —21-year-old man with cystic fibrosis, multilobular biliary
cirrhosis, and slightly elevated liver enzyme levels. High-resolution sonogram
of liver surface shows irregular margin with lobulation (arrow) due
to scarring. Scale segment distance, 5 mm.
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Fig. 8A —23-year-old man with cystic fibrosis, multilobular biliary
cirrhosis, and portal hypertension. Longitudinal sonogram of left lobe of
liver shows small liver with irregular margin. Ascites (star) next to
liver is evident. Scale segment distance, 10 mm.
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Fig. 8B —23-year-old man with cystic fibrosis, multilobular biliary
cirrhosis, and portal hypertension. Color Doppler sonogram obtained at same
level as A shows numerous vessels (arrow) within minor
omentum, representing portosystemic collateral vessels. Star indicates
ascites.
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Fig. 8D —23-year-old man with cystic fibrosis, multilobular biliary
cirrhosis, and portal hypertension. Longitudinal sonogram shows marked
enlargement of spleen, measuring 19 cm in length, indicating portal
hypertension.
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Biliary Tract
Cholesterol gallstones, often within a shrunken gallbladder
(microgallbladder) occur in as many as 12% of children and young adults with
CF [3] (Figs.
9,
10, and
11). These abnormalities are
not usually associated with symptoms. As in sclerosing cholangitis, the
intrahepatic bile duct abnormalities include strictures, dilatation, and
ductal calculi [2] (Figs.
12A and
12B). These abnormalities can
be evaluated with sonography, and color Doppler mode can be helpful for
differentiating vessels and bile duct (Figs.
12A and
12B), but MR cholangiography
is more accurate for diagnosis
[2].
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Fig. 9 —6-year-old boy with asymptomatic microgallbladder.
Longitudinal sonogram shows example of biliary abnormality in fasting patient
with cystic fibrosis. Small, empty gallbladder (GB) (arrow) is 25 mm
long. Scale segment distance, 10 mm.
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Fig. 10 —9-year-old boy with sludge (arrow) within small
gallbladder. Sonogram shows example of biliary abnormality in fasting patient
with cystic fibrosis. Echogenic fat tissue surrounds gallbladder.
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Fig. 11 —16-year-old girl with asymptomatic cholelithiasis.
Longitudinal sonogram of gallbladder shows example of biliary abnormality in
fasting patient with cystic fibrosis. Microgallbladder containing multiple
shadowing echogenic calculi (arrowhead) and mild diffuse thickening
of gallbladder wall (arrow) are evident.
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Fig. 12A —11-year-old boy with asymptomatic cystic fibrosis and
dilatation of intrahepatic bile duct. Transverse high-resolution B-mode
(A) and color Doppler (B) sonograms of left lobe of liver show
dilated bile duct (arrowhead) beside hepatic artery (star)
and portal vein (arrow). Scale segment distance, 5 mm. VP = portal
vein, BD = bile duct, AH = hepatic artery.
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Fig. 12B —11-year-old boy with asymptomatic cystic fibrosis and
dilatation of intrahepatic bile duct. Transverse high-resolution B-mode
(A) and color Doppler (B) sonograms of left lobe of liver show
dilated bile duct (arrowhead) beside hepatic artery (star)
and portal vein (arrow). Scale segment distance, 5 mm. VP = portal
vein, BD = bile duct, AH = hepatic artery.
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Gastrointestinal Tract
A variety of abnormalities of gastrointestinal function, such as meconium
ileus, distal intestinal obstruction syndrome, intussusception, mucoid
appendix, and fibrosing colonopathy, can occur in CF. Meconium ileus occurs in
10–15% of newborns with CF, and it is the earliest clinical
manifestation of CF [1]. The
obstruction is caused by impaction of inspissated meconium in the terminal
ileum. A small colon associated with proximal small-bowel distention is the
typical sonographic finding (Figs.
13A and
13B). However, identical
findings are seen in small-bowel atresia unrelated to CF. Although meconium
ileus can be detected with sonography, the standard of reference is abdominal
radiography followed by contrast enema for diagnosis and treatment. As many as
one half of cases of meconium ileus are complicated by volvulus, atresia, or
meconium peritonitis [3].
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Fig. 13A —1-day-old boy with cystic fibrosis and meconium ileus.
Transverse (A) and longitudinal (B) high-resolution sonograms
show small descending colon with diminished caliber (microcolon)
(arrows) and dilated, meconium-filled small bowel (star).
Scale segment distance, 5 mm. s = spleen, k = kidney, sp = spine.
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Fig. 13B —1-day-old boy with cystic fibrosis and meconium ileus.
Transverse (A) and longitudinal (B) high-resolution sonograms
show small descending colon with diminished caliber (microcolon)
(arrows) and dilated, meconium-filled small bowel (star).
Scale segment distance, 5 mm. s = spleen, k = kidney, sp = spine.
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The term distal intestinal obstruction syndrome, previously called meconium
ileus equivalent, is applied to intestinal impaction and partial or complete
obstruction in older patients
[3]. Abdominal pain, a palpable
right lower quadrant abdominal mass, and bowel obstruction are the most common
symptoms and signs. Large amounts of fecal material in the ileocecal region
may be visible at sonography (Figs.
14A and
14B). Contrast enema
examinations not only help to define the fecal mass but also may relieve the
obstruction. CT is not indicated for the diagnosis or management of this
entity.
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Fig. 14A —10-month-old girl with cystic fibrosis and distal intestinal
obstruction syndrome. Abdominal radiograph obtained with patient in left
recumbent position shows right colon filled with fecal mass (star)
and multiple air-filled levels within dilated small bowel.
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Fig. 14B —10-month-old girl with cystic fibrosis and distal intestinal
obstruction syndrome. Transverse sonogram of right lower quadrant shows
dilated bowel loaded with fecal material (star). Scale segment
distance, 5 mm
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Intussusception affects approximately 1% of patients with CF. It is most
frequently ileocolic and can occur as a complication of distal intestinal
obstruction syndrome [2].
Sonography readily depicts intussusception, showing the target sign of
edematous bowel and intermixed mesenteric fat on transverse images
[3]. In the absence of
perforation or signs of peritonitis, hydrostatic enema can be performed under
sonographic guidance to reduce the intussusceptum
[1].
Transient asymptomatic small-bowel intussusception, usually jejunal, is
seen in as many as 5% of CF patients
[8] (Figs.
15A and
15B). Unlike those of
ileocolic intussusception, the intussuscepta are small in diameter, short
(< 5 cm), and usually central in the abdomen or in the left upper quadrant.
In patients with no symptoms in whom no definitive pathologic lead point is
recognized on imaging, conservative observation is warranted. Intermittent
sonographic examinations over a 45-minute period may reveal spontaneous
reduction of this benign type of intussusception
[9].
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Fig. 15A —3-year-old girl with asymptomatic cystic fibrosis and
small-bowel intussusception. Transverse high-resolution sonogram of left upper
quadrant shows multiple concentric ring sign of jejunal intussusception caused
by entering and returning limbs of infolded intussusceptum. Star-shaped center
(star) represents transverse section of infolded jejunal loop of
intussusceptum. Scale segment distance, 5 mm.
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Fig. 15B —3-year-old girl with asymptomatic cystic fibrosis and
small-bowel intussusception. Longitudinal sonogram shows short-segment
intussusception (length, 10 mm). Entering and returning wall of intussusceptum
(arrows) is known as sandwich sign. Spontaneous reduction was found
during real-time sonographic examination.
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Abnormalities of the appendix are found in as many as 16% of patients with
asymptomatic CF. These abnormalities include swollen and distended mucoid
appendix caused by inspissated mucoid contents (Figs.
16A and
16B). Progress to acute
appendicitis is rare, occurring in 1–4% of CF patients in comparison
with 7% of the general population
[2]. However, differentiating
acute appendicitis from chronically distended, mucoid appendix with imaging
alone may be especially difficult in patients with CF, resulting in delayed
diagnosis and a high rate of appendiceal perforation and abscess formation.
These complications can be detected with sonography, but CT is more accurate
for diagnosis.
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Fig. 16A —9-year-old girl with asymptomatic cystic fibrosis and mucoid
appendix. Transverse (A) and longitudinal (B) high-resolution
sonograms at level of right psoas muscle show swollen appendix (diameter, 9
mm) with hypoechoic luminal contents (star) corresponding to
inspissated mucoid secretions. Small amount of free fluid is present. Linear
echogenic appearance of preserved submucosal layer (arrows, B)
and lack of periappendiceal inflammatory changes are evident. Scale segment
distance, 5 mm.
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Fig. 16B —9-year-old girl with asymptomatic cystic fibrosis and mucoid
appendix. Transverse (A) and longitudinal (B) high-resolution
sonograms at level of right psoas muscle show swollen appendix (diameter, 9
mm) with hypoechoic luminal contents (star) corresponding to
inspissated mucoid secretions. Small amount of free fluid is present. Linear
echogenic appearance of preserved submucosal layer (arrows, B)
and lack of periappendiceal inflammatory changes are evident. Scale segment
distance, 5 mm.
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The colon is often abnormal in patients with CF
[8]. Fibrosing colonopathy is a
well-described feature in CF patients, particularly in children taking
high-strength pancreatic enzyme supplements. The condition is characterized by
marked fibrosis of the submucosa and predominantly involves the proximal
portion of the colon. In severe cases, colonic stricture and obstruction
occur. Colonic shortening, focal or extensive narrowing, and poor
distensibility during contrast-enhanced enema studies are considered highly
suggestive of the prestricture state
[3]. Sonography is a means of
detecting mucosal changes and bowel-wall thickening and has supplemented the
conventional diagnostic methods, that is, barium enema and endoscopy
[8]. Submucosal bowelwall
thickening is visualized on sonography in as many as 81% of patients with
asymptomatic CF (Figs. 17A and
17B). In severe cases, the
findings probably represent a sonomorphologic correlate of an early stage of
fibrosing colonopathy [8].
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Fig. 17A —15-year-old boy with asymptomatic cystic fibrosis and colonic
wall thickening. Transverse (A) and longitudinal (B)
high-resolution sonograms of ascending colon show fecal content
(star) within lumen and pronounced (4.5 mm) nodular thickening
(double arrow) of wall with increased thickness of echogenic
submucosal layer (arrow). Pericolonic fat proliferation
(arrowhead, B) is evident. Scale segment distance, 5 mm.
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Fig. 17B —15-year-old boy with asymptomatic cystic fibrosis and colonic
wall thickening. Transverse (A) and longitudinal (B)
high-resolution sonograms of ascending colon show fecal content
(star) within lumen and pronounced (4.5 mm) nodular thickening
(double arrow) of wall with increased thickness of echogenic
submucosal layer (arrow). Pericolonic fat proliferation
(arrowhead, B) is evident. Scale segment distance, 5 mm.
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Conclusion
Gastrointestinal involvement in CF predisposes patients to morbid
conditions. Numerous gastrointestinal complications develop with sonographic
manifestations that must be interpreted correctly to ensure appropriate
therapy. In addition to careful clinical and laboratory examinations of each
patient, sonography may aid in the management of the disease.
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Abstract
Introduction
