Cystic Fibrosis in Children and Young Adults: Findings on Routine Abdominal Sonography
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1 bdominal Sonography in Cystic Fibrosis bdominal Imaging Pictorial Essay Downloaded from by on 01/08/18 from IP address Copyright RRS. For personal use only; all rights reserved Hans P. Haber 1 Haber HP Keywords: cystic fibrosis, liver disease, pancreaticobiliary imaging, pediatric imaging, small bowel, sonography DOI: /JR Received ugust 8, 2006; accepted after revision January 15, Department of Pediatrics, University of Tuebingen, Hoppe-Seyler-Str. 1, D Tuebingen, Germany. ddress correspondence to H. P. Haber (peter.haber@med.uni-tuebingen.de). JR 2007; 189: X/07/ merican Roentgen Ray Society Cystic Fibrosis in Children and Young dults: Findings on Routine bdominal Sonography OJECTIVE. 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. ystic fibrosis (CF) is the most common lethal genetic defect in white C populations [1]. iochemical 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]. ecause of diagnostic and therapeutic advances, life expectancy has lengthened. 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]. bdominal sonography, used commonly in the diagnostic evaluation, can depict abnormalities of the pancreas, liver, gallbladder, spleen, and bowel. wareness 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 ntares, Siemens Medical Solutions) had 7.5-MHz curved array and highresolution 12-MHz linear array probes. Pancreas y 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. 1 and 2). Hypoechoic areas representing pancreatic fibrosis sometimes are found, as are pancreatic calcifications and small pancreatic cysts measuring 1 3 mm (Fig. 3). Pancreatic cystosis, complete replacement of the pancreas by cysts, is well depicted with sonography, CT, and MRI [6] (Fig. 4). 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. 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 JR:189, July
2 Downloaded from by on 01/08/18 from IP address Copyright RRS. For personal use only; all rights reserved (Fig. 5). There is no evidence to suggest that steatosis progresses to cirrhosis [2]. 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 (Fig. 6). The sonographic findings may precede clinical and biochemical evidence of liver disease. pproximately 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 (Fig. 7). When portal hypertension develops, splenic enlargement, portosystemic collateral vessels, and, occasionally, ascites are seen on sonography [4] (Fig. 8). iliary 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 11). These abnormalities are not usually associated with symptoms. s in sclerosing cholangitis, the intrahepatic bile duct abnormalities include strictures, dilatation, and ductal calculi [2] (Fig. 12). These abnormalities can be evaluated with sonography, and color Doppler mode can be helpful for differentiating vessels and bile duct (Fig. 12), but MR cholangiography is more accurate for diagnosis [2]. Gastrointestinal Tract 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. small colon associated with proximal small-bowel distention is the typical sonographic finding (Fig. 13). However, identical findings are seen in smallbowel atresia unrelated to CF. lthough meconium ileus can be detected with sonography, the standard of reference is abdominal radiography followed by contrast enema for diagnosis and treatment. s many as one half of cases of meconium ileus are complicated by volvulus, atresia, or meconium peritonitis [3]. 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]. bdominal 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 (Fig. 14). 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. 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] (Fig. 15). 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]. bnormalities 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 (Fig. 16). 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. 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 contrastenhanced 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 (Fig. 17). In severe cases, the findings probably represent a sonomorphologic correlate of an early stage of fibrosing colonopathy [8]. 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. References 1. Milla PJ. Cystic fibrosis: present and future. Digestion 1998; 59: Robertson M, Choe K, Joseph PM. Review of the abdominal manifestations of cystic fibrosis in the adult patient. RadioGraphics 2006; 26: grons G, Corse WR, Markowitz RI, et al. Gastrointestinal manifestations of cystic fibrosis: radiologic-pathologic correlation. RadioGraphics 1996; 16: Chaudry G, Navarro OM, Levine DS, Oudjhane K. bdominal manifestations of cystic fibrosis in children. Pediatr Radiol 2006; 36: Philips HE, Cox KL, Reidl MH, McGahan JP. Pancreatic sonography in cystic fibrosis. JR 1981; 137: errocal T, Pajares MP, Zubillaga F. Pancreatic cystosis in children and young adults with cystic fibrosis: sonographic, CT, and MRI findings. JR 2005; 184: De oeck K, Weren M, Proesmans M, Kerem E. Pancreatitis among patients with cystic fibrosis: correlation with pancreatic status and genotype. Pediatrics 2005; 115: Haber HP, enda N, Fitzke G, et al. Colonic wall thickness measured by ultrasound: striking differences in patients with cystic fibrosis versus healthy controls. Gut 1997; 40: Kornecki, Daneman, Navarro O, et al. Spontaneous reduction of intussusception: clinical spectrum, management and outcome. Pediatr Radiol 2000; 30: JR:189, July 2007
3 bdominal Sonography in Cystic Fibrosis Downloaded from by on 01/08/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig. 1 9-year-old boy with cystic fibrosis and pancreatic exocrine insufficiency. and, Longitudinal () and transverse () sonograms at level of pancreatic head show small pancreas (arrows) with areas of markedly increased echogenicity, resembling echogenicity of retroperitoneal fat (star, ). Scale segment distance, 10 mm. s = superior mesenteric artery, ao = aorta. Fig. 2 9-year-old boy in good health. and, Longitudinal () and transverse () sonograms show normal pancreas (arrows) for comparison with Figure 1. Pancreatic echogenicity is equivalent to that of liver. Scale segment distance, 10 mm. Star indicates retroperitoneal fat. ao = aorta, vci = inferior vena cava. JR:189, July
4 Downloaded from by on 01/08/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig 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., xial contrast-enhanced T1-weighted MR image obtained at same level as shows intermixed low signal intensity (arrow) representing pancreatic fibrosis. Fig year-old boy with asymptomatic cystic fibrosis and pancreatic cystosis. and, Longitudinal () and transverse () 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. 92 JR:189, July 2007
5 bdominal Sonography in Cystic Fibrosis Downloaded from by on 01/08/18 from IP address Copyright RRS. For personal use only; all rights reserved C Fig. 5 5-year-old girl with cystic fibrosis, hepatic steatosis, and slightly elevated liver enzyme levels. Scale segment distance, 10 mm. and, Longitudinal () and transverse () 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 throughtransmission is evident. C, High-resolution sonogram through right lobe of liver shows poor visualization of portal triads (arrows). JR:189, July
6 Downloaded from by on 01/08/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig 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., High-resolution sonogram of liver shows irregular echotexture and hyperechoic periportal thickening (arrows) due to presence of focal fat. Fig 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., High-resolution sonogram of liver surface shows irregular margin with lobulation (arrow) due to scarring. Scale segment distance, 5 mm. 94 JR:189, July 2007
7 bdominal Sonography in Cystic Fibrosis Downloaded from by on 01/08/18 from IP address Copyright RRS. For personal use only; all rights reserved C Fig 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. scites (star) next to liver is evident. Scale segment distance, 10 mm., Color Doppler sonogram obtained at same level as shows numerous vessels (arrow) within minor omentum, representing portosystemic collateral vessels. Star indicates ascites. C, Pulsed Doppler image shows hepatofugal flow within varices. D, Longitudinal sonogram shows marked enlargement of spleen, measuring 19 cm in length, indicating portal hypertension. D JR:189, July
8 Downloaded from by on 01/08/18 from IP address Copyright RRS. For personal use only; all rights reserved 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 (G) (arrow) is 25 mm long. Scale segment distance, 10 mm. Fig 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. Fig 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. 96 JR:189, July 2007
9 bdominal Sonography in Cystic Fibrosis Downloaded from by on 01/08/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig year-old boy with asymptomatic cystic fibrosis and dilatation of intrahepatic bile duct. and, Transverse high-resolution -mode () and color Doppler () 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, D = bile duct, H = hepatic artery. Fig day-old boy with cystic fibrosis and meconium ileus. and, Transverse () and longitudinal () high-resolution sonograms show small descending colon with diminished caliber (microcolon) (arrows) and dilated, meconiumfilled small bowel (star). Scale segment distance, 5 mm. s = spleen, k = kidney, sp = spine. JR:189, July
10 Downloaded from by on 01/08/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig month-old girl with cystic fibrosis and distal intestinal obstruction syndrome., bdominal 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., Transverse sonogram of right lower quadrant shows dilated bowel loaded with fecal material (star). Scale segment distance, 5 mm Fig 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., 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. 98 JR:189, July 2007
11 bdominal Sonography in Cystic Fibrosis Downloaded from by on 01/08/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig year-old girl with asymptomatic cystic fibrosis and mucoid appendix. and, Transverse () and longitudinal () 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, ) and lack of periappendiceal inflammatory changes are evident. Scale segment distance, 5 mm. Fig year-old boy with asymptomatic cystic fibrosis and colonic wall thickening. and, Transverse () and longitudinal () 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, ) is evident. Scale segment distance, 5 mm. JR:189, July
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