Radiology
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Published online before print January 17, 2007, 10.1148/radiol.2423050784
This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
2423050784v1
242/3/759    most recent
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kim, S. H.
Right arrow Articles by Choi, B. I.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kim, S. H.
Right arrow Articles by Choi, B. I.
(Radiology 2007;242:759-768.)
© RSNA, 2007

Gastrointestinal Imaging

Esophageal Varices in Patients with Cirrhosis: Multidetector CT Esophagography—Comparison with Endoscopy1

Se Hyung Kim, MD, Yoon Jun Kim, MD, Jeong Min Lee, MD, Kee Don Choi, MD, Young Jin Chung, MD, Joon Koo Han, MD, Jae Young Lee, MD, Min Woo Lee, MD, Chang Jin Han, MD, Joon Il Choi, MD, Kyung-Sook Shin, MD and Byung Ihn Choi, MD

1 From the Department of Radiology (S.H.K., J.M.L., J.K.H., J.Y.L., M.W.L., C.J.H., J.I.C., K.S.S., B.I.C.), Institute of Radiation Medicine (J.M.L., J.K.H., B.I.C.), Department of Internal Medicine (Y.J.K., K.D.C., Y.J.C.), and Liver Research Institute (Y.J.K., Y.J.C.), Seoul National University Hospital, 28 Yongon-dong, Chongno-gu, Seoul 110-744, Korea; and Chungnam National University Hospital, Deajeon, Korea (K.S.S.). Received May 8, 2005; revision requested July 6; revision received March 2, 2006; accepted April 28; final version accepted June 23. Address correspondence to Y.J.K. (e-mail: yoonjun{at}snu.ac.kr).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Purpose: To evaluate the use of multidetector computed tomographic (CT) esophagography to grade esophageal varices and differentiate between varices at low risk and those at high risk for bleeding, with endoscopy as the reference standard.

Materials and Methods: This study was approved by the institutional review board; all subjects gave informed consent. Ninety patients with cirrhosis (65 men, 25 women; mean age, 54.8 years; range, 21–77 years) were prospectively enrolled and underwent endoscopy and CT esophagography. Esophageal varices were graded independently at endoscopy by two endoscopists. CT esophagograms were interpreted retrospectively with a four-point scale by two radiologists blinded to other findings. Interobserver agreement between each radiologist and endoscopist was determined; endoscopic and CT esophagographic grades of esophageal varices were correlated. Radiologist performance for differentiation between low- and high-risk varices for bleeding on the basis of morphology at endoscopy was evaluated with receiver operating characteristic analysis. Patients were interviewed to determine acceptance at both examinations.

Results: Thirty-seven of 90 patients had grade 0, 23 had grade 1, 18 had grade 2, and 12 had grade 3 esophageal varices. Thus, 60 patients were determined to be in a low-risk group and 30 in a high-risk group for variceal bleeding at endoscopy. There was almost perfect agreement in grading esophageal varices between endoscopists. There was close correlation (P < .001) and substantial agreement between endoscopic and CT esophagographic grades. Radiologist performance for differentiating between low- and high-risk varices was 0.931–0.958 (area under receiver operating characteristic curve). Patient interview results revealed that CT esophagography had better acceptance than did endoscopy (P < .001).

Conclusion: Use of CT esophagography allows grading of esophageal varices and differentiation between low- and high-risk varices and shows better patient acceptance than does endoscopy.

© RSNA, 2007


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
The prevalence of esophageal varices in patients with cirrhosis has been reported to be 80%–90% (1,2), and patients with esophageal varices develop variceal hemorrhage at a rate of 10%–30% per year (3). Despite substantial improvements in the early diagnosis and treatment of variceal hemorrhage, the mortality of variceal hemorrhage remains high (20%–35%) (4–6).

Many clinicians advocate the use of screening endoscopy for decreasing the risk of variceal bleeding and for detection of esophageal varices at the initial diagnosis of cirrhosis and every 1–3 years thereafter (3,4). Results of several studies have demonstrated that the development or progression of esophageal varices can be treated successfully and further esophageal bleeding can be prevented by using ß-blockers or endoscopic variceal ligation (2,4,7,8); consequently, the mortality of patients with cirrhosis can be reduced (9). There is a general consensus with regard to the viability of a strategy of screening endoscopy followed by prophylactic treatment of the varices (10). However, there has been debate regarding whether endoscopic screening for esophageal varices in cirrhotic patients is cost-effective for the primary prophylaxis of variceal bleeding (10–12).

As well as the development of varices, hepatocellular carcinoma (HCC) is another major complication of cirrhosis. Therefore, routine surveillance of cirrhotic patients with abdominal ultrasonography (US) and {alpha}-fetoprotein (AFP) levels has been widely practiced (13). According to results of a recent report (14) on the cost-effectiveness of surveillance for HCC in cirrhotic patients, biannual AFP and annual computed tomographic (CT) screening may be comparably cost-effective to biannual AFP screening and annual US. Routine surveillance of cirrhotic patients for both varices and HCC necessitates multiple diagnostic tests, including US or CT and AFP screening, as well as endoscopy. Considering the high cost of performing multiple tests and the relative invasiveness of endoscopy, a single noninvasive surveillance tool for both varices and HCC may be important.

With the advances in multidetector CT and the three-dimensional (3D) imaging technique, combined interpretation of two-dimensional transverse and 3D images can be easily performed, and, consequently, diagnostic capabilities are enhanced (15,16). Thus, the purpose of our study was to evaluate the use of multidetector CT esophagography to grade esophageal varices and differentiate between varices at low risk and those at high risk for bleeding, with endoscopy as the reference standard.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Patient Population
From August to November 2004, 142 consecutive cirrhotic patients who were scheduled to undergo surveillance or follow-up CT for HCC were prospectively evaluated for inclusion in the study. The diagnosis of cirrhosis was made on the basis of liver histologic findings (n = 11) or the combination of typical clinical features (symptoms and stigmata of cirrhosis and its complications), laboratory results (of viral marker, hyperbilirubinemia, hypoalbuminemia, coagulopathy, and cytopenia testing), and imaging findings (liver configuration, splenomegaly, ascites, and collateral vessels) (n = 131). Patients with active gastrointestinal hemorrhage, those with a history of endoscopic variceal ligation, those with a history of adverse reactions to iodinated contrast agent, and those who refused to enroll in the study were excluded. After the exclusions, 90 patients were included. Patient demographics, causes of cirrhosis, and Child-Pugh classes are given in Table 1. This study had approval from the institutional review board of Seoul National University Hospital. Informed consent was obtained from all patients.


View this table:
[in this window]
[in a new window]

  		Table 1. Characteristics of 90 Patients with Cirrhosis

 
Endoscopy
All patients underwent standard endoscopy performed by one of four gastroenterologists (Y.J.K., with 14 years of experience; three others with 5, 10, and 18 years of experience). On the basis of the gastroenterology policy at our institute, intravenous sedation was not induced in any patient. All endoscopic studies were captured as Digital Imaging and Communications in Medicine files and were reviewed independently at a picture archiving and communication system by two gastroenterologists (K.D.C. and Y.J.C., both with 8 years of experience) who did not participate in the endoscopic examination and who were unaware of the patient's physical findings, laboratory values, and CT esophagographic findings. They determined the grade of esophageal varices. The grading system was used according to criteria proposed by the Japanese Research Society for Portal Hypertension (17) (Table 2). The patients were divided into two groups (low and high risk) on the basis of their probability for developing an esophageal variceal hemorrhage. A grade of 2 or higher was chosen as the cutoff point to define high-risk varices (1,18,19). Discrepancies in the interpretations between the endoscopists were resolved by consensus after the independent reading. This occurred in 16 cases.


View this table:
[in this window]
[in a new window]

  		Table 2. Grading System for Esophageal Varices Proposed by Japanese Research Society for Portal Hypertension

 
Multidetector CT Imaging
All patients underwent CT esophagography within 4 hours after endoscopy. CT esophagography was performed with a 16-detector CT scanner (Sensation 16; Siemens Medical Systems, Forchheim, Germany). Before CT examination, 10 mg of butyl scopolamine (Buscopan; Boehringer Ingelheim, Seoul, Korea) was administered intravenously to facilitate hypotonia. For air insufflation, a 16-F end-hole catheter, which was connected to a mechanical inflator (Enema Teleflator CK-85; Kaigen, Osaka, Japan) beside the CT console with a long plastic connector, was inserted into the upper esophagus through the mouth. Air injection was performed by one radiologist (S.H.K.) at a rate of 700 mL/30 sec from 12 seconds before scanning to the time the scanner passed the gastroesophageal junction during the arterial and portal phases. Patients were informed that adequate esophageal distention with air insufflation is important to obtain good CT esophagographic images; therefore, they were asked not to belch during air insufflation. However, if the patient complained of discomfort, air injection was stopped immediately. The total amount of injected air was recorded.

Three CT phases, including precontrast scanning, were performed by using the following parameters: section collimation, 0.75 mm; section thicknesses, 1 mm (for arterial and portal phases) and 3 mm; table feed, 12 mm per rotation; rotation time, 0.5 second per rotation; 160 mAs; and 120 kVp. For the precontrast phase, air injection was not used and images were acquired of the liver. For arterial and portal phases, two scanning passes were performed from the entire thorax and abdomen to the iliac wing. Arterial and portal phase images were reconstructed at an interval of 0.7 mm to obtain a high-quality data set for CT esophagographic reconstruction and were also reconstructed at an interval of 3 mm for routine evaluation. Each scanning pass was about 18 seconds. The scanning delay was 6 and 20 seconds after achieving enhancement of the descending aorta up to 100 HU for the arterial and portal phases, respectively. One hundred twenty milliliters of nonionic contrast material (iopromide, Ultravist 300; Schering, Berlin, Germany) was intravenously administered at a rate of 4 mL/sec.

Just after CT scanning, a high-quality data set with a 0.7-mm reconstruction interval was transferred to a personal computer with dedicated 3D software (Rapidia, version 2.8; Infinitt, Seoul, Korea). One of four radiologic technologists with experience in 3D techniques (two with 5 years of experience, two with 7 years of experience) reconstructed CT images with a volume-rendering technique by using surface-shaded, transparent, and endoscopic modes. Reconstructed 3D images were sent to a picture archiving and communication system as Digital Imaging and Communications in Medicine files.

Analysis of CT Esophagographic Results
Two reviewers (J.M.L. and J.Y.L., with 13 and 11 years of experience, respectively) retrospectively evaluated 3D CT esophagographic images by consensus for the degree of esophageal distention. The esophagus was divided into three segments (upper, middle, and lower). The degree of distention in the different esophageal segments was graded by using the following three-point scale: a score of 1 indicated more than 75% of expected maximal luminal dimension (good distention), a score of 2 indicated 51%–75% of expected maximal luminal dimension (fair distention), and a score of 3 indicated less than 50% of expected maximal luminal dimension (poor distention) (20).

The grade of esophageal varices was independently assessed by two other gastrointestinal radiologists (S.H.K. and K.S.S., with 5 and 9 years of experience, respectively) who were blinded to the patient's physical findings, laboratory values, previous imaging results, and endoscopic results. Before the interpretation session, radiologists underwent a training session by using 10 cases with various grades of esophageal varices. The cases in the training session were not included in the interpretation session.

The esophagus was surveyed by using both two-dimensional transverse and 3D images at a picture archiving and communication system workstation. The grading system had the same classification as that used at standard endoscopy (17) (Table 2). The radiologists also assigned one of five confidence level ratings (1 = definitely low risk, 2 = probably low risk, 3 = possibly high risk, 4 = probably high risk, and 5 = definitely high risk) for the development of variceal bleeding on the basis of endoscopic findings that are correlated with variceal bleeding. A grade 2 rating or higher was chosen as the cutoff point to define high-risk varices (1,18,19). To evaluate intraobserver variability, a similar interpretation session was performed 2 weeks after the first interpretation session.

Additionally, two reviewers (S.H.K., K.S.S.) evaluated transverse CT images by consensus to diagnose extraesophageal abnormalities. They recorded the presence of paraesophageal or gastric submucosal varices, HCCs, splenomegaly, and ascites according to previously published criteria (21–25).

Patient Acceptance
To evaluate patient acceptance of the procedure, we questioned patients immediately after each procedure regarding their global discomfort, pain, and other symptoms (eg, gagging, belching, and abdominal fullness) with the following four-point scale: 1, none; 2, mild; 3, moderate; or 4, severe. Patient acceptance was also evaluated by asking each patient whether he or she would be reluctant to repeat the examination if it were necessary with the following scale: 1 indicated "yes", 2 indicated "no", or 3 indicated "I don't know." Finally, all patients were asked which of the two examinations they preferred (26,27). To avoid bias, all queries were made by using forms and without a human assisting the patient.

Statistical Analysis
CT esophagographic grades given by the radiologists were correlated with the endoscopic grades given by the endoscopists by using weighted {kappa} statistics and the Spearman correlation. We considered a {kappa} value of more than 0.81 to represent almost perfect agreement and values of 0.61–0.80 and 0.41–0.60 to represent substantial and moderate agreement, respectively. Values of less than 0.40 were considered to represent fair agreement (28). Interobserver agreement between the endoscopists with regard to the endoscopic interpretation and inter- and intraobserver agreement between the radiologists for each session of CT esophagographic interpretation also were evaluated by using weighted {kappa} statistics (28).

The degree of distention among the three esophageal segments was compared by using the Fisher exact test. The individual performances of radiologists with respect to differentiating between low-risk and high-risk varices for bleeding for both sessions were evaluated and compared by using the area under the receiver operating characteristic curve (Az). In addition, sensitivity and specificity of CT esophagography for assessing high-risk varices on the basis of endoscopic findings that are correlated with variceal bleeding (reference standard) were determined and compared with the Fisher exact test.

The tolerability of CT esophagography was compared with that of endoscopy by using the Student t test. The willingness to repeat the examination was compared with the Fisher exact test. For all tests, a P value of less than .05 indicated a statistically significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Endoscopy
Thirty-nine and 37 of 90 patients were classified as having grade 0 esophageal varices by endoscopists 1 and 2, respectively. Twenty-four and 23 patients were classified as having grade 1, 19 and 18 were classified as having grade 2, and eight and 12 were classified as having grade 3 esophageal varices by endoscopists 1 and 2, respectively. The weighted {kappa} value for agreement between the endoscopists was 0.831, which represented almost perfect agreement. When the endoscopists reached consensus for 16 discrepant cases, 37 (41%) of 90 patients were classified as having grade 0, 23 (26%) were classified as having grade 1, 18 (20%) were classified as having grade 2, and 12 (13%) were classified as having grade 3 esophageal varices. Resolving the discrepancies by consensus did not affect the statistical results. Finally, 60 (67%) patients were categorized into a low-risk group and 30 (33%) into a high-risk group for variceal bleeding at endoscopy.

CT Esophagography
Esophageal distention.—Mean volume of injected air was 1289 mL (range, 810–1860 mL). Total grades for the distention of the three esophageal segments are summarized in Table 3 (Figs 1–3). The degree of distention among the three esophageal segments was significantly different (P < .001). For two patients who received a poor grade in the lower esophagus, transverse CT images played a main role in the determination of the grades of esophageal varices.


View this table:
[in this window]
[in a new window]

  		Table 3. Distention Grades Assigned to Three Esophageal Segments in 90 Patients

 

Figure 1A
View larger version (42K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1a: Images in 61-year-old woman with cirrhosis but no esophageal varices. (a) Surface-shaded volume-rendered and (b) virtual endoscopic CT images demonstrate a suspicious linear elevated structure (arrows). On a, esophageal distention was graded as good throughout entire esophagus. Note mild indentation (arrowhead) of middle esophageal segment due to extrinsic compression by heart. (c) Transverse CT scan reveals no enhanced vessels within esophageal wall. Therefore, final variceal grade recorded by the two radiologists was 0. Note enhanced paraesophageal varices (arrows) around esophagus. (d) Conventional endoscopic image confirms that there are no varices in esophagus.

 

Figure 1B
View larger version (115K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1b: Images in 61-year-old woman with cirrhosis but no esophageal varices. (a) Surface-shaded volume-rendered and (b) virtual endoscopic CT images demonstrate a suspicious linear elevated structure (arrows). On a, esophageal distention was graded as good throughout entire esophagus. Note mild indentation (arrowhead) of middle esophageal segment due to extrinsic compression by heart. (c) Transverse CT scan reveals no enhanced vessels within esophageal wall. Therefore, final variceal grade recorded by the two radiologists was 0. Note enhanced paraesophageal varices (arrows) around esophagus. (d) Conventional endoscopic image confirms that there are no varices in esophagus.

 

Figure 1C
View larger version (120K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1c: Images in 61-year-old woman with cirrhosis but no esophageal varices. (a) Surface-shaded volume-rendered and (b) virtual endoscopic CT images demonstrate a suspicious linear elevated structure (arrows). On a, esophageal distention was graded as good throughout entire esophagus. Note mild indentation (arrowhead) of middle esophageal segment due to extrinsic compression by heart. (c) Transverse CT scan reveals no enhanced vessels within esophageal wall. Therefore, final variceal grade recorded by the two radiologists was 0. Note enhanced paraesophageal varices (arrows) around esophagus. (d) Conventional endoscopic image confirms that there are no varices in esophagus.

 

Figure 1D
View larger version (126K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1d: Images in 61-year-old woman with cirrhosis but no esophageal varices. (a) Surface-shaded volume-rendered and (b) virtual endoscopic CT images demonstrate a suspicious linear elevated structure (arrows). On a, esophageal distention was graded as good throughout entire esophagus. Note mild indentation (arrowhead) of middle esophageal segment due to extrinsic compression by heart. (c) Transverse CT scan reveals no enhanced vessels within esophageal wall. Therefore, final variceal grade recorded by the two radiologists was 0. Note enhanced paraesophageal varices (arrows) around esophagus. (d) Conventional endoscopic image confirms that there are no varices in esophagus.

 

Figure 2A
View larger version (25K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2a: Grade 2 esophageal varices in lower esophageal segment in 58-year-old man with cirrhosis and concomitant gastric submucosal varices and HCC. (a) Surface-shaded volume-rendered and (b, c) virtual endoscopic CT images demonstrate large varices (arrows) with a beaded appearance in lower segment and concomitant gastric submucosal varices (arrowhead) in gastric fundus. GE = gastroesophageal junction. On a, distention was graded as good throughout entire esophagus. (d) Transverse CT image obtained at level of hepatic hilum during arterial phase demonstrates two enhanced nodules with fuzzy margins (arrows) in segment VIII of liver. These lesions were confirmed as HCCs with celiac angiography and subsequent contrast material–enhanced CT. (e) On transverse CT image obtained at level of gastric fundus during portal venous phase, these lesions (arrows) show isoattenuation and low attenuation. Note enhanced gastric submucosal varices (arrowhead). (f) Conventional endoscopic image confirms grade 2 esophageal varices (arrows).

 

Figure 2B
View larger version (97K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2b: Grade 2 esophageal varices in lower esophageal segment in 58-year-old man with cirrhosis and concomitant gastric submucosal varices and HCC. (a) Surface-shaded volume-rendered and (b, c) virtual endoscopic CT images demonstrate large varices (arrows) with a beaded appearance in lower segment and concomitant gastric submucosal varices (arrowhead) in gastric fundus. GE = gastroesophageal junction. On a, distention was graded as good throughout entire esophagus. (d) Transverse CT image obtained at level of hepatic hilum during arterial phase demonstrates two enhanced nodules with fuzzy margins (arrows) in segment VIII of liver. These lesions were confirmed as HCCs with celiac angiography and subsequent contrast material–enhanced CT. (e) On transverse CT image obtained at level of gastric fundus during portal venous phase, these lesions (arrows) show isoattenuation and low attenuation. Note enhanced gastric submucosal varices (arrowhead). (f) Conventional endoscopic image confirms grade 2 esophageal varices (arrows).

 

Figure 2C
View larger version (102K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2c: Grade 2 esophageal varices in lower esophageal segment in 58-year-old man with cirrhosis and concomitant gastric submucosal varices and HCC. (a) Surface-shaded volume-rendered and (b, c) virtual endoscopic CT images demonstrate large varices (arrows) with a beaded appearance in lower segment and concomitant gastric submucosal varices (arrowhead) in gastric fundus. GE = gastroesophageal junction. On a, distention was graded as good throughout entire esophagus. (d) Transverse CT image obtained at level of hepatic hilum during arterial phase demonstrates two enhanced nodules with fuzzy margins (arrows) in segment VIII of liver. These lesions were confirmed as HCCs with celiac angiography and subsequent contrast material–enhanced CT. (e) On transverse CT image obtained at level of gastric fundus during portal venous phase, these lesions (arrows) show isoattenuation and low attenuation. Note enhanced gastric submucosal varices (arrowhead). (f) Conventional endoscopic image confirms grade 2 esophageal varices (arrows).

 

Figure 2D
View larger version (58K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2d: Grade 2 esophageal varices in lower esophageal segment in 58-year-old man with cirrhosis and concomitant gastric submucosal varices and HCC. (a) Surface-shaded volume-rendered and (b, c) virtual endoscopic CT images demonstrate large varices (arrows) with a beaded appearance in lower segment and concomitant gastric submucosal varices (arrowhead) in gastric fundus. GE = gastroesophageal junction. On a, distention was graded as good throughout entire esophagus. (d) Transverse CT image obtained at level of hepatic hilum during arterial phase demonstrates two enhanced nodules with fuzzy margins (arrows) in segment VIII of liver. These lesions were confirmed as HCCs with celiac angiography and subsequent contrast material–enhanced CT. (e) On transverse CT image obtained at level of gastric fundus during portal venous phase, these lesions (arrows) show isoattenuation and low attenuation. Note enhanced gastric submucosal varices (arrowhead). (f) Conventional endoscopic image confirms grade 2 esophageal varices (arrows).

 

Figure 2E
View larger version (53K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2e: Grade 2 esophageal varices in lower esophageal segment in 58-year-old man with cirrhosis and concomitant gastric submucosal varices and HCC. (a) Surface-shaded volume-rendered and (b, c) virtual endoscopic CT images demonstrate large varices (arrows) with a beaded appearance in lower segment and concomitant gastric submucosal varices (arrowhead) in gastric fundus. GE = gastroesophageal junction. On a, distention was graded as good throughout entire esophagus. (d) Transverse CT image obtained at level of hepatic hilum during arterial phase demonstrates two enhanced nodules with fuzzy margins (arrows) in segment VIII of liver. These lesions were confirmed as HCCs with celiac angiography and subsequent contrast material–enhanced CT. (e) On transverse CT image obtained at level of gastric fundus during portal venous phase, these lesions (arrows) show isoattenuation and low attenuation. Note enhanced gastric submucosal varices (arrowhead). (f) Conventional endoscopic image confirms grade 2 esophageal varices (arrows).

 

Figure 2F
View larger version (112K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2f: Grade 2 esophageal varices in lower esophageal segment in 58-year-old man with cirrhosis and concomitant gastric submucosal varices and HCC. (a) Surface-shaded volume-rendered and (b, c) virtual endoscopic CT images demonstrate large varices (arrows) with a beaded appearance in lower segment and concomitant gastric submucosal varices (arrowhead) in gastric fundus. GE = gastroesophageal junction. On a, distention was graded as good throughout entire esophagus. (d) Transverse CT image obtained at level of hepatic hilum during arterial phase demonstrates two enhanced nodules with fuzzy margins (arrows) in segment VIII of liver. These lesions were confirmed as HCCs with celiac angiography and subsequent contrast material–enhanced CT. (e) On transverse CT image obtained at level of gastric fundus during portal venous phase, these lesions (arrows) show isoattenuation and low attenuation. Note enhanced gastric submucosal varices (arrowhead). (f) Conventional endoscopic image confirms grade 2 esophageal varices (arrows).

 

Figure 3A
View larger version (45K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 3a: Images of grade 3 esophageal varices in lower esophagus in 60-year-old man with cirrhosis. (a) Surface-shaded volume-rendered and (b) virtual endoscopic CT images demonstrate tumorlike varices (arrows) with tortuosity in lower esophagus. On a, distention was graded as good in lower esophageal segments and as poor in upper and middle segments. Transverse CT images can demonstrate enhanced esophageal varices but do not show morphologic characteristics of tortuous appearance and obliquity of esophageal varices. (c) Conventional endoscopic image confirms grade 3 esophageal varices.

 

Figure 3B
View larger version (127K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 3b: Images of grade 3 esophageal varices in lower esophagus in 60-year-old man with cirrhosis. (a) Surface-shaded volume-rendered and (b) virtual endoscopic CT images demonstrate tumorlike varices (arrows) with tortuosity in lower esophagus. On a, distention was graded as good in lower esophageal segments and as poor in upper and middle segments. Transverse CT images can demonstrate enhanced esophageal varices but do not show morphologic characteristics of tortuous appearance and obliquity of esophageal varices. (c) Conventional endoscopic image confirms grade 3 esophageal varices.

 

Figure 3C
View larger version (134K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 3c: Images of grade 3 esophageal varices in lower esophagus in 60-year-old man with cirrhosis. (a) Surface-shaded volume-rendered and (b) virtual endoscopic CT images demonstrate tumorlike varices (arrows) with tortuosity in lower esophagus. On a, distention was graded as good in lower esophageal segments and as poor in upper and middle segments. Transverse CT images can demonstrate enhanced esophageal varices but do not show morphologic characteristics of tortuous appearance and obliquity of esophageal varices. (c) Conventional endoscopic image confirms grade 3 esophageal varices.

 
Diagnostic performance of CT esophagography.—CT esophagographic grades determined by radiologists during each session, when compared with the grades determined by the endoscopists (Table 4, Figs 1–3), shared close correlation and substantial agreement (Table 5). Table 5 also presents the results of linear regression that demonstrate the correlation between CT esophagographic and endoscopic grades.


View this table:
[in this window]
[in a new window]

  		Table 4. CT Esophagographic Grades of Esophageal Varices Determined by Radiologists during Each Session and Endoscopic Grades Determined by Endoscopists

 

View this table:
[in this window]
[in a new window]

  		Table 5. Interobserver Agreement and Correlation between Endoscopists and Radiologists for Each Session and Linear Regression Results

 
For interobserver agreement between the radiologists, substantial ({kappa} = 0.760) and almost perfect ({kappa} = 0.801) agreementwere achieved for the first and second interpretation sessions, respectively. For intraobserver agreement, substantial ({kappa} = 0.758) agreement for radiologist 1 and almost perfect ({kappa} = 0.818) agreement for radiologist 2 were achieved between the interpretation sessions of grading esophageal varices.

The performance of the radiologists for differentiation of low-risk and high-risk varices for bleeding was 0.931–0.958 for Az, 90%–93.3% for sensitivity, and 81.7%–96.7% for specificity, regardless of the interpretation session (Table 6). The differences in Az, sensitivity, and specificity of the radiologists were not statistically significant for either session (P > .05).


View this table:
[in this window]
[in a new window]

  		Table 6. Radiologist Performance for Differentiating between Low- and High-Risk Esophageal Varices with Regard to the Propensity to Bleed

 
Extraesophageal abnormalities.—In 60 of 90 patients, extraesophageal abnormalities were found as follows: HCC in 10 (Fig 2), paraesophageal varices in 25, gastric submucosal varices in 27 (Fig 2), splenomegaly in 55, ascites in two, and benign cyst of the posterior mediastinum in one.

Patient Acceptance
The responses for CT esophagography (Table 7) were significantly more favorable than those for endoscopy (P < .001). For willingness to undergo repeat examination, patients were significantly less reluctant to undergo repeat CT esophagography than repeat endoscopy (P = .007). Sixty of 90 patients responded that they preferred CT esophagography to endoscopy, and 13 patients preferred endoscopy. The remaining 17 patients had no preference.


View this table:
[in this window]
[in a new window]

  		Table 7. Grades Assigned by 90 Patients to Two Modalities with Respect to Patient Acceptance and Comparative Statistical Analysis Results

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 References
 
In our study, the sensitivity and specificity for predicting high-risk esophageal varices were approximately 93% and 97%, respectively. Furthermore, the performance of the radiologists for predicting high-risk esophageal varices was 0.931–0.958 for Az. Considering that the final goal of endoscopic screening for esophageal varices is to decrease mortality and morbidity due to esophageal variceal bleeding, we suggest that our results have clinical importance. However, with respect to intra- and interobserver agreement between the interpretation sessions and the radiologists, the results were worse than those of the endoscopists. We believe a major factor that explains this finding is the unfamiliarity of the radiologists with endoscopic images of the esophagus.

As with CT colonography, with CT esophagography, adequate distention of the esophagus is essential for creating high-quality 3D images. One of the reasons for the high-performance results in our study is related to a careful technique for distending the esophagus. We achieved esophageal distention through air insufflation by using intubation and a mechanical inflator. As a result, most of the esophageal segments—in particular the upper esophagus, as well as the lower esophagus, in which most esophageal varices developed—were well distended, and the resulting 3D images were adequate for variceal evaluation. For the middle esophagus, however, we had some difficulties obtaining adequate distention in a substantial proportion of patients. This finding can be explained by the extrinsic compression caused by the heart. Another group (29), however, simply used an effervescent agent to achieve esophageal dilatation. It is anticipated that the use of an effervescent agent will further increase patient compliance. However, as the authors mentioned in their report, the technique required considerable patient cooperation to achieve optimal distention of the esophagus. Good CT esophagographic images cannot be obtained without highly cooperative patients. For this issue, further studies that compare the use of a mechanical insufflator with that of an effervescent agent are needed.

As a minimally invasive procedure, CT esophagography provides many advantages when compared with standard endoscopy. First, it allows accurate localization of the varices due to the depiction of extraesophageal anatomic landmarks. Second, in light of the lack of consensus with regard to the role of screening endoscopy in cirrhotic patients due to low cost-effectiveness, CT esophagography might replace screening endoscopy because clinicians can be provided with information regarding both esophageal varices and HCC. Consequently, time and money could be saved if patients underwent CT esophagography. However, an investigation seems warranted to evaluate the cost-effectiveness of CT esophagography for dual screening of esophageal varices and HCC in cirrhotic patients. Finally, CT esophagography appears to be superior to endoscopy for depiction of extraesophageal abnormalities, as demonstrated in our study. Although other risk factors such as splenomegaly, portal vein diameter greater than or equal to 15 mm, ascites, HCC, and gastric submucosal varices confer a higher risk of variceal bleeding (30–32), detection of extraesophageal abnormalities by using CT esophagography may, in itself, give further information about the propensity of esophageal variceal bleeding.

With respect to patient acceptance, we found that the preference for CT esophagography was significantly greater than that for endoscopy. However, as we continue to use intubation for luminal distention, there must be room for further improvement. If a more effective effervescent agent can be developed, a further increase in patient preference could be achieved for CT esophagography without intubation.

There are some limitations of CT esophagography when compared with endoscopy for the screening of esophageal varices. First, the qualitative endoscopic appearance (ie, the presence of red signs) cannot be assessed at CT esophagography. Red signs at endoscopy represent protruded reddish spots or bands overlying varices. Such signs can be predictors of both variceal bleeding and varices at high risk for bleeding (19). The second disadvantage of CT esophagography is that therapeutic intervention cannot be performed, whereas this is possible during endoscopy. Finally, there is an increased risk of radiation hazard due to the increased coverage used at CT esophagography compared with the coverage used at a routine liver CT examination. Considering that the evaluation of esophageal varices is focused on the distal esophagus, scanning starting from the lower rather than from the upper esophagus may lessen the radiation hazard. In addition, use of a dose modulation program in both the transverse and z-axis directions may help further reduce the radiation dose.

There were some limitations to our study. First, we used static endoscopic images rather than videoscopic images to evaluate esophageal varices. Because varices are effaced by inflating the lumen, they should be evaluated in a dynamic fashion. However, this shortcoming can be overcome by a review of several static images because our protocol included several images in which the esophagus was distended or collapsed. Second, we did not obtain long-term follow-up data regarding whether the patients evaluated with CT esophagography eventually had esophageal variceal bleeding.

In conclusion, our investigation demonstrated that the use of CT esophagography allows grading of esophageal varices, as well as differentiation between low- and high-risk varices with regard to propensity for bleeding. CT esophagography might thus be an alternative tool for evaluation of esophageal varices. Compared with endoscopy, CT esophagography gives additional information regarding extraesophageal abnormalities and is preferred more by patients due to its less invasive nature.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
References
 


   FOOTNOTES
 

Abbreviations: Az = area under the receiver operating characteristic curve • HCC = hepatocellular carcinoma • 3D = three-dimensional

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, S.H.K., Y.J.K., B.I.C.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, S.H.K., Y.J.K., J.K.H., J.I.C.; clinical studies, S.H.K., Y.J.K., J.M.L., K.D.C., Y.J.C., J.Y.L., K.S.S.; statistical analysis, M.W.L., C.J.H.; and manuscript editing, Y.J.K., J.M.L., J.K.H., J.Y.L., M.W.L., J.I.C., K.S.S., B.I.C.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 

  1. Lay CS, Tsai YT, Teg CY, et al. Endoscopic variceal ligation in prophylaxis of first variceal bleeding in cirrhotic patients with high-risk esophageal varices. Hepatology 1997;25:1346–1350.[CrossRef][Medline]
  2. D'Amico G, Pagliaro L, Bosch J. Pharmacological treatment of portal hypertension: an evidence-based approach. Semin Liver Dis 1999;19:475–505.[Medline]
  3. Garcia-Tsao G. Current management of the complications of cirrhosis and portal hypertension: variceal hemorrhage, ascites, and spontaneous bacterial peritonitis. Gastroenterology 2001;120:726–748.[CrossRef][Medline]
  4. Pagliaro L, D'Amico G, Sorensen TI, et al. Prevention of first bleeding in cirrhosis: a meta-analysis of randomized trials of nonsurgical treatment. Ann Intern Med 1992;117:59–70.[Abstract/Free Full Text]
  5. Sarin SK, Lamba GS, Kumar M, Misra A, Murthy NS. Comparison of endoscopic ligation and propranolol for the primary prevention of variceal bleeding. N Engl J Med 1999;340:988–993.[Abstract/Free Full Text]
  6. D'Amico G, Pagliaro L, Bosch J. The treatment of portal hypertension: a meta-analytic review. Hepatology 1995;22:332–354.[CrossRef][Medline]
  7. De BK, Ghoshal UC, Das T, Santra A, Biswas PK. Endoscopic variceal ligation for primary prophylaxis of oesophageal variceal bleed: preliminary report of a randomized controlled trial. J Gastroenterol Hepatol 1999;14:220–224.[CrossRef][Medline]
  8. Schepke M, Kleber G, Nurnberg D, et al. Ligation versus propranolol for the primary prophylaxis of variceal bleeding in cirrhosis. Hepatology 2004;40:65–72.[CrossRef][Medline]
  9. Tripathi D, Hayes PC. Review article: a drug therapy for the prevention of variceal haemorrhage. Aliment Pharmacol Ther 2001;15:291–310.[CrossRef][Medline]
  10. Spiegel BM, Targownik L, Dulai GS, Karsan HA, Gralnek IM. Endoscopic screening for esophageal varices in cirrhosis: is it ever cost effective? Hepatology 2003;37:366–377.[CrossRef][Medline]
  11. Teran JC, Imperiale TF, Mullen KD, Tavill AS, McCullough AJ. Primary prophylaxis of variceal bleeding in cirrhosis: a cost-effectiveness analysis. Gastroenterology 1997;112:473–482.[CrossRef][Medline]
  12. Aoki N, Kajiyama T, Beck JR, Cone RW, Soma K, Fukui T. Decision analysis of prophylactic treatment for patients with high-risk esophageal varices. Gastrointest Endosc 2000;52:707–714.[CrossRef][Medline]
  13. Chalasani N, Said A, Ness R, Hoen H, Lumeng L. Screening for hepatocellular carcinoma in patients with cirrhosis in the United States: results of a national survey. Am J Gastroenterol 1999;94:2224–2229.[CrossRef][Medline]
  14. Lin OS, Keeffe EB, Sanders GD, Owens DK. Cost-effectiveness of screening for hepatocellular carcinoma in patients with cirrhosis due to chronic hepatitis C. Aliment Pharmacol Ther 2004;19:1159–1172.[CrossRef][Medline]
  15. Pickhardt PJ, Choi JR, Hwang I, et al. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. N Engl J Med 2003;349:2191–2200.[Abstract/Free Full Text]
  16. Kim SH, Han JK, Lee KH, Chung JW, Yang HK, Choi BI. Computed tomography gastrography with volume-rendering technique: correlation with double-contrast barium study and conventional gastroscopy. J Comput Assist Tomogr 2003;27:140–149.[CrossRef][Medline]
  17. Idezuki Y. General rules for recording endoscopic findings of esophagogastric varices (1991). Japanese Society for Portal Hypertension. World J Surg 1995;19:420–422.
  18. Prediction of the first variceal hemorrhage in patients with cirrhosis of the liver and esophageal varices: a prospective multicenter study. The North Italian Endoscopic Club for the Study and Treatment of Esophageal Varices. N Engl J Med 1988;319:983–989.[Abstract]
  19. Beppu K, Inokuchi K, Koyanagi N, et al. Prediction of variceal hemorrhage by esophageal endoscopy. Gastrointest Endosc 1981;27:213–218.[Medline]
  20. Griffith JF, Kew J, Chan AC, Metreweli C. 3D CT imaging of oesophageal carcinoma. Eur J Radiol 1999;32:216–220.[CrossRef][Medline]
  21. Balthazar EJ, Naidich DP, Megibow AJ, Lefleur RS. CT evaluation of esophageal varices. AJR Am J Roentgenol 1987;148:131–135.[Abstract/Free Full Text]
  22. Willmann JK, Weishaupt D, Bohm T, et al. Detection of submucosal gastric fundal varices with multi-detector row CT angiography. Gut 2003;52:886–892.[Abstract/Free Full Text]
  23. Yamashita Y, Mitsuzaki K, Yi T, et al. Small hepatocellular carcinoma in patients with chronic liver damage: prospective comparison of detection with dynamic MR imaging and helical CT of the whole liver. Radiology 1996;200:79–84.[Abstract/Free Full Text]
  24. Prassopoulos P, Daskalogiannaki M, Raissaki M, Hatjidakis A, Gourtsoyiannis N. Determination of normal splenic volume on computed tomography in relation to age, gender and body habitus. Eur Radiol 1997;7:246–248.[CrossRef][Medline]
  25. Bruix J, Sherman M, Llovet JM, et al. Clinical management of hepatocellular carcinoma: conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 2001;35:421–430.
  26. Frommer D. Cleansing ability and tolerance of three bowel preparations for colonoscopy. Dis Colon Rectum 1997;40:100–104.[CrossRef][Medline]
  27. Lefere PA, Gryspeerdt SS, Dewyspelaere J, Baekelandt M, Van Holsbeeck BG. Dietary fecal tagging as a cleansing method before CT colonography: initial results—polyp detection and patient acceptance. Radiology 2002;224:393–403.[Abstract/Free Full Text]
  28. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159–174.[CrossRef][Medline]
  29. Mazzeo S, Caramella D, Gennai A, et al. Multidetector CT and virtual endoscopy in the evaluation of the esophagus. Abdom Imaging 2004;29:2–8.[Medline]
  30. Chalasani N, Imperiale TF, Ismail A, et al. Predictors of large esophageal varices in patients with cirrhosis. Am J Gastroenterol 1999;94:3285–3291.[CrossRef][Medline]
  31. Akanuma M, Yoshida H, Okamoto M, et al. Risk factors for esophageal variceal bleeding in patients with hepatocellular carcinoma. Hepatogastroenterology 2002;49:1039–1044.[Medline]
  32. Thomopoulos KC, Labropoulou-Karatza C, Mimidis KP, Katsakoulis EC, Iconomou G, Nikolopoulou VN. Non-invasive predictors of the presence of large oesophageal varices in patients with cirrhosis. Dig Liver Dis 2003;35:473–478.[CrossRef][Medline]



This article has been cited by other articles:


Home page
 RadioGraphicsHome page
Y. K. Kim, Y. Kim, and S. S. Shim
Thoracic Complications of Liver Cirrhosis: Radiologic Findings
RadioGraphics, May 1, 2009; 29(3): 825 - 837.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Roentgenol.Home page
S. H. Kim, J. M. Lee, J. Y. Choi, K.-S. Suh, N.-J. Yi, J. K. Han, and B. I. Choi
Changes of Portosystemic Collaterals and Splenic Volume on CT After Liver Transplantation and Factors Influencing Those Changes
Am. J. Roentgenol., July 1, 2008; 191(1): W8 - W16.
[Abstract] [Full Text] [PDF]

Home page
 RadiologyHome page
C.-H. Liu, S.-J. Hsu, C.-C. Liang, F.-C. Tsai, J.-W. Lin, C.-J. Liu, P.-M. Yang, M.-Y. Lai, P.-J. Chen, J.-H. Chen, et al.
Esophageal Varices: Noninvasive Diagnosis with Duplex Doppler US in Patients with Compensated Cirrhosis
Radiology, July 1, 2008; 248(1): 132 - 139.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
2423050784v1
242/3/759    most recent
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kim, S. H.
Right arrow Articles by Choi, B. I.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kim, S. H.
Right arrow Articles by Choi, B. I.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
RADIOLOGY RADIOGRAPHICS RSNA JOURNALS ONLINE