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(Radiology. 1999;211:229-232.)
© RSNA, 1999

Pediatric Imaging

Liver Disease in Children with Cystic Fibrosis: US-Biochemical Comparison in 195 Patients1

Heidi Patriquin, MD, Catherine Lenaerts, MD, Lesley Smith, MD, Gilles Perreault, MD, Andrée Grignon, MD, Denis Filiatrault, MD, Jacques Boisvert, MD, Claude C. Roy, MD and Andrée Rasquin-Weber, MD

1 From the Departments of Medical Imaging (H.P., G.P., A.G., D.F., J.B.) and Gastroenterology (C.L., L.S., C.C.R., A.R.W.), Sainte-Justine Hospital, 3175 Côte Ste-Catherine, Montreal, Quebec, H3T 1C5, Canada. Received December 24, 1997; revision requested March 24, 1998; revision received August 3; accepted October 13. Supported in part by grants from the Justine-Lacoste-Beaubien Foundation. Address reprint requests to H.P.


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To determine if abnormal liver architecture at ultrasonography (US) is related to abnormal function in children with cystic fibrosis (CF).

MATERIALS AND METHODS: For 1 year, all 195 children (112 boys, 83 girls; mean age, 8.5 years) attending a CF clinic underwent abdominal US and a standard set of liver function tests. Aspartate aminotransferase, alanine aminotransferase, and {gamma}-glutamyltransferase levels were analyzed. US signs were interpreted as follows: hypoechogenicity with prominent portal tracks as edema, hyperechogenicity as steatosis, and increased attenuation and nodules within or at the edge of the liver as cirrhosis. Signs of portal hypertension also were sought. US signs were compared with liver function test results.

RESULTS: Liver sonograms were abnormal in 38 children (19%); of these, 24 (63%) had abnormal test results. The 157 children with normal liver architecture had a much lower prevalence of biochemical abnormality (33 patients [21%]; P <= .001). All eight children with signs of portal hypertension had abnormal test results. Fourteen (82%) of 17 children with signs of cirrhosis had abnormal liver function. Eight (57%) of 14 patients with signs of steatosis had abnormal function. Diffuse hypoechogenicity of the liver with prominent portal tracks in 16 patients was associated with abnormal function in only five patients.

CONCLUSION: The relation between abnormal liver architecture at US and results of three liver function tests in children with CF was significant. The most specific US abnormalities related to abnormal function are signs suggestive of portal hypertension and cirrhosis.

Index terms: Fibrosis, cystic, 761.1496 • Hypertension, portal, 95.711 • Liver, cirrhosis, 761.794 • Liver, US, 761.12983 • Ultrasound (US), in infants and children, 761.12983


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
With improved survival of children with cystic fibrosis (CF), the hepatobiliary manifestations of the disease present an important diagnostic and therapeutic challenge. Clinical manifestations are usually present only in relatively advanced disease (1). A means of detecting or predicting liver disease at an early stage is desirable to effectively direct treatment. Ultrasonography (US) is used as one of several tests to assess liver disease in such children. We wished to determine if liver architecture at US is related to abnormal liver function, as measured with biochemical tests.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
For 1 year, all 195 children (112 boys, 83 girls; age range, 1–23 years; mean age, 8.5 years) in a CF clinic undergoing routine blood tests for liver function underwent the following protocol: abdominal US to assess liver architecture, a standard set of liver function tests, and a clinical examination. Abdominal US and biochemical tests were performed on the same day. Informed consent was obtained from the patients or families. The study was approved by the hospital committee on ethics and human experimentation.

US scans were obtained without sedation after a 4-hour fast in children aged 2–6 years and after an 8-hour fast in patients older than 6 years. One of the following commercially available machines was used: Ultramark 5, 8, or 9 (Advanced Technology Laboratories, Seattle, Wash) or Quantum II (Siemens Medical Systems, Erlangen, Germany) with a 3.5-, 5.0-, or 7.0-MHz transducer. The sonograms were obtained by one of five pediatric radiologists (H.P., G.P., A.G., D.F., J.B.) and were later reviewed by one of the five. No radiologist was aware of the biochemical results at the time of examination or review. US included a survey of the entire abdomen as well as a detailed examination of liver architecture. This included liver echogenicity, which was compared with that of the renal cortex. The liver was called hyperechoic if it was brighter than the cortex of the right kidney and if the walls of portal veins were difficult to distinguish from the adjacent liver parenchyma (2). Sound attenuation by the liver was assessed and was considered to be increased if the posterior surface of the liver was not visible with a transducer frequency that allowed sound penetration and depiction of the kidney through the liver. Evidence of nodules within and at the surface of the liver was sought. The caliber of the intrahepatic bile ducts was noted, and they were termed dilated if they exceeded 2 mm in diameter. Evidence of portal hypertension was sought (splenomegaly, collateral veins, lesser omental thickening); when found, Doppler US was performed. The presence and direction of blood flow in the splanchnic and intrahepatic portal veins was assessed, and portosystemic collateral vessels, especially esophageal varices (3), were sought.

US abnormalities of liver architecture were interpreted as follows: hyperechogenicity as steatosis (2) and heteroechogenicity of liver architecture accompanied by increased sound attenuation as cirrhosis (4,5). Nodules within or at the edge of the liver were also interpreted as cirrhosis. Hypoechoic liver parenchyma and bright periportal echoes of normal thickness also were noted, but no pathologic interpretation was attributed to these findings.

Clinical parameters obtained at the time of the study included height, weight, weight-to-height ratio (as a percentage), and Shwachman score within 1 month of US. The Shwachman scoring system is the one most commonly used to assess the clinical status of children with CF. In this scoring system, a maximum of 25 points is given for each of the following parameters: physical activity, nutrition, physical examination, chest radiographs. The lower the score, the worse the clinical condition, since points are deducted for deterioration (6). Liver function tests included total and direct bilirubin, aspartate aminotransferase (AST), alanine aminotransferase (ALT), {gamma}-glutamyltransferase (GGT), albumin, prealbumin, prothrombin time, and fasting and postprandial endogenous bile acid (cholylglycine) tests. Relationships between the prevalence of sonographically abnormal liver architecture and the prevalence of abnormal liver function test results were sought by using the {chi}2 test and accepting a P value less than .01 as significant.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
US Findings
The initial sonologist (G.P., A.G., D.F., J.B.) and the reviewer (H.P.) agreed on the interpretation of liver and bile duct sonograms in 189 of the 195 children. In the remaining six children, there was minor disagreement on the degree but not on the nature of liver echogenicity. In 38 patients (19%; 25 boys, 13 girls), liver US scans were abnormal. The patients with abnormal US scans were older (10.8 years ± 4.6) than the rest of the patients with CF (7.8 years ± 4.3).

A partly or completely hyperechoic liver with nearly normal sound attenuation suggestive of steatosis was seen in 14 patients (Fig 1). Heterogeneous echogenicity of the liver with nodules and increased sound attenuation suggestive of cirrhosis was seen in 17 of the 38 patients (Fig 2); in seven of these, biopsy was performed and results showed biliary cirrhosis. Eight of the 17 children with signs of cirrhosis also had US signs of portal hypertension (3) (Fig 3). Six of the 38 patients had diffuse hypoechoic areas in the liver, with bright periportal tissues of normal thickness. Mild intrahepatic bile duct dilatation was seen in one of the 38 patients with biopsy-proved cirrhosis and portal hypertension, but subsequent transvesicular cholangiography failed to show evidence of bile duct stenosis.



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  		Figure 1. Steatosis, with focal sparing, in a 16-year-old girl with CF. Sagittal sonogram shows the right kidney (short straight arrow), gallbladder (curved arrow), and hyperechoic liver parenchyma with islands of tissue of normal echogenicity (long straight arrow), especially near the portal vein and gallbladder.

 


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  		Figure 2. Cirrhosis in a 16-year-old boy with CF. Oblique coronal subcostal sonogram shows heterogeneous liver architecture. Nodules are visible within the liver and at its edge. The path of the portal veins is deformed by the nodules (open arrow). A hyperechoic area (solid arrow) in the liver probably represents steatosis.

 


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  		Figure 3. Portal hypertension in an 18-year-old girl with CF. Sagittal Doppler sonogram shows the aorta (thick arrow) and the nodular contour of the left lobe (arrowhead) of the liver. Between these structures, blood flow (blue Doppler signals) within the left gastric vein is hepatofugal and directed toward the esophagus (thin arrow).

 
Biochemical Findings
The AST level was elevated in 51 (26%) of the 195 patients; the ALT level, in 29 patients (15%); and the GGT level, in 31 patients (16%). Other liver parameters, including the serum total and direct bilirubin levels, the prothrombin time, and the cholylglycine level were abnormal in up to 25 (13%) of the 195 patients. The serum albumin level was decreased in 25 (13%) and the prealbumin level was decreased in 37 (19%) of the 195 patients, but these results were associated with malnutrition. The AST, ALT, and GGT levels were selected for study analysis since they represented the liver function test results most often found to be abnormal.

Twenty-four (63%) of the 38 children with abnormal liver sonograms had abnormal liver function test results. Thirty-three (21%) of the 157 children with normal liver sonograms had abnormal liver function (Table 1). This difference between the two groups reached statistical significance (P < .001); children with sonographically abnormal livers had a much higher prevalence of abnormal liver function.


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  		TABLE 1. Association of Abnormal Liver US Findings with Clinical and Biochemical Findings in 195 Patients
 
The association of these liver function test results with specific subtypes of liver US abnormalities was examined more closely. These findings are shown in Table 2. Six patients with diffuse hypoechoic areas in the liver and prominent periportal tissue showed little evidence of liver enzyme abnormality. Of the 14 patients with US evidence of steatosis, 57% had abnormal liver enzyme levels. Of the 17 patients with US signs of cirrhosis, 82% had abnormal enzyme levels. All eight children with US and Doppler evidence of portal hypertension had abnormal enzyme levels.


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  		TABLE 2. Association of Subtypes of US Liver Abnormalities with Abnormal Enzyme Levels
 

   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Cystic fibrosis is a recessively inherited disease caused by a defective gene on the long arm of chromosome 7 (7). This gene, called CFTR (cystic fibrosis transmembrane chloride regulator) (8), codes for a protein that functions as a regulated epithelial chloride channel and is responsible for the normal passage of chloride at the luminal surface of epithelial cells (9). When the gene is defective, chloride secretion is reduced; at the same time, there is increased reabsorption of sodium from cell secretions (10). Since water follows the movement of salt, thick secretions are formed that may lead to obstruction (8,11,12). In the liver, these abnormal secretions are probably involved in the development of biliary cirrhosis, which becomes more severe as the child ages. At microscopy, inspissated bile secretions are seen, forming eosinophilic plugs that obstruct small bile ducts. Ductular proliferation is followed by inflammation and fibrosis. At autopsy, steatosis and focal or multinodular cirrhosis are seen (13–15).

Clinical signs of cirrhosis in children with CF occur late, even when the disease is advanced. Some patients present with hemorrhage from previously unsuspected gastroesophageal varices (1). A recently developed clinical score to predict liver disease in CF showed a sensitivity of 85% and a specificity of 82%, but the exact nature of the hepatic lesions could not be predicted (16). It is noteworthy that this score included clinical factors and liver enzyme levels but no US evaluation. By outlining the liver architecture, US potentially adds precision about the prevalence and nature of liver disease in children with CF.

Abdominal US has the advantage of being rapid, noninvasive, relatively cheap, and sensitive in the detection of liver and biliary tract abnormalities. It may also be repeated on many occasions. Doppler examination enhances the diagnostic yield by providing further information about the portal circulation. In our hands, the interpretation of liver sonograms was remarkably reproducible among five different pediatric radiologists. Evaluation of the accuracy of US in detecting liver disease in patients with CF is best done by means of comparison with histopathologic findings. Routine liver biopsy was not possible in our children for medical and ethical reasons. We therefore compared our results with liver function test results. Those most frequently abnormal were GGT, AST, and ALT levels, and the relation between US and function was based on measurements of these three enzyme levels.

Thirty-eight (19%) of our patients had abnormal liver architecture at US, and this prevalence agrees with that in other series of similarly aged patients (17–21). Fourteen (7%) of our patients had US signs of steatosis, a lower prevalence than the 30% reported at autopsy (13). Eight of these children (57%) had abnormal enzymes. Steatosis and cirrhosis coexist as the liver disease of CF advances. We made the US diagnosis of steatosis only when we could see no nodules and sound attenuation was normal. (None of these children underwent liver biopsy, since they were relatively healthy.) US evidence of cirrhosis was found in 17 (8.7%) of the 195 patients, a figure that is identical to the prevalence of cirrhosis in a French population of 2,400 patients with CF (22). Fourteen (82%) of these children had abnormal enzymes. One-half of patients in our study with US evidence of cirrhosis also had signs of portal hypertension. All had abnormal enzyme levels. Three of these children have had one or more episodes of variceal bleeding and have been treated with sclerotherapy. This prevalence contrasts with that in the adult CF population studied by Graham et al (23); in that study, nearly all the patients with abnormal liver US findings also had evidence of portal hypertension, which likely reflects their more advanced disease.

In six patients, we noted a hypoechoic liver, with bright periportal tissues of normal thickness. Two had abnormal enzyme levels. The importance of this finding remains obscure in our patients. In one of our patients, there was evidence of mild intrahepatic bile duct dilatation. No stenosis or obstruction was noted at cholangiography. Like O'Brien et al (24), we have been unable to confirm the work of Gaskin et al (25), who suggested that stenosis of the hepatic or common bile ducts might be an etiologic factor in liver disease in patients with cystic fibrosis (26).

Researchers in few studies to date have attempted to relate US liver architecture to liver function in patients with CF. In a study with 35 adults, Graham et al (23) found no relation between liver US (abnormal echogenicity, sound attenuation, and nodules) and function (serum alkaline phosphatase, GGT, and AST levels). Quillin et al (21) examined 27 children with CF. Although the majority (63%) had abnormal liver sonograms, Quillin et al could find no relation to function, measured as serum alkaline phosphatase, AST, and ALT levels. McHugo et al (17) found nodules at the inferior edge of the liver in 17 of 76 children with CF. Fourteen of these children had abnormal alkaline phosphatase, AST, ALT, and GGT levels. These results are similar to ours in children with cirrhosis.

Williams et al (27) examined 68 adults with CF and devised a scoring system of US liver abnormalities: Coarse or irregular parenchyma, nodular liver edge, and periportal fibrosis (thickened, hyperechoic periportal tissues) were each given a score of 0–3 points. A US score exceeding 3 was considered abnormal. High scores were related to long spleens, large splenic venous diameters, and a higher prevalence of clinical hepatosplenomegaly, palmar erythema, and gynecomastia and to abnormal results of biochemical tests of liver function, especially alkaline phosphatase, GGT, ALT, AST, and serum bilirubin levels. The authors then examined 16 prepubertal children with CF and noted that the same US signs could be found in these children.

Our study was performed prior to the 1995 publication of the Williams scoring system. US evaluation of liver architecture in the two studies is similar, even though the descriptive terms differ. Our heterogeneous livers correspond to the descriptions and photographs of "irregular parenchyma" and "increased periportal echogenicity" in the article by Williams et al (27). The descriptions of nodules are similar in the two studies. However, Williams et al (27) do not mention or illustrate hyperechoic livers, which we found and interpreted as steatosis, perhaps because the adults examined had more advanced disease (cirrhosis). Neither study was based on liver histology, but the results of small numbers of biopsies in each substantiated the US diagnosis of cirrhosis on the basis of visible liver nodules.

Our prospective study revealed that abnormalities of liver architecture and function are common in children with CF and that their prevalence increases with age. As in the study by Williams et al (27) in adults, we found that abnormal liver architecture (especially signs of portal hypertension and nodular liver architecture) is related to abnormal function (particularly, abnormal GGT, ALT, and AST levels). Liver disease in patients with CF is clinically silent until the disease is advanced. Periodic US and biochemical function tests may provide indicators of liver disease in these children before complications occur.


   Acknowledgments
 
Our thanks go to Marie-Claude Guertin, MSc, for advice on statistics, to Denise Collins, DEC, for illustrations, and to Lucie Martinelli, DEC, and Diane Lefebvre, DEC, for preparing the manuscript.


   Footnotes
 
Abbreviations: ALT = alanine aminotransferase AST = aspartate aminotransferase CF = cystic fibrosis GGT = {gamma}-glutamyltransferase

Author contributions: Guarantors of integrity of entire study, H.P., A.R.W.; study concepts, A.R.W., H.P.; study design, H.P., A.R.W., C.L.; definition of intellectual content, H.P., C.L., C.C.R.; literature research, H.P., A.R.W.; clinical studies, H.P., D.F., C.L., A.G., J.B., G.P.; data acquisition, H.P., C.L., L.S.; data analysis, H.P., L.S.; statistical analysis, H.P.; manuscript preparation, H.P., L.S.; manuscript editing and review, H.P., A.R.W.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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