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1 Department of Radiology, Osaka City University Graduate School of Medicine,
1-4-3 Asahi-machi, Abeno-ku, Osaka 545-8585, Japan.
2 Department of Radiology, Faculty of Medicine, Tottori University, Yonago,
Japan.
3 Department of Gastroenterology, Osaka City University Graduate School of
Medicine, Osaka, Japan.
Received May 1, 2004;
accepted after revision August 12, 2004.
Address correspondence to T. Ninoi
(ninoi{at}msic.med.osaka-cu.ac.jp).
Abstract
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MATERIALS AND METHODS. A total of 78 patients with cirrhosis and with gastric varices, successfully treated by B-RTO, were enrolled in this study. Recurrence and bleeding of gastric varices and worsening of esophageal varices were endoscopically evaluated. Univariate and multivariate analyses were used to assess the prognostic factors for worsening of esophageal varices and survival.
RESULTS. Recurrence of gastric varices was found in two patients; the 5-year recurrence rate was 2.7%. Bleeding of gastric varices occurred in only one patient after B-RTO; the 5-year bleeding rate was 1.5%. Worsening of esophageal varices was observed in 29 patients, and the worsening rates at 1, 3, and 5 years were 27%, 58%, and 66%, respectively. These esophageal varices were endoscopically treated to prevent rupture. Multivariate analysis showed the presence of esophageal varices before B-RTO was a prognostic factor for worsening (relative risk, 4.956). At a median follow-up of 700 days (range, 137-2,339 days), the survival rates at 1, 3, and 5 years were 93%, 76%, and 54%, respectively. The prognostic factors associated with survival were presence of hepatocellular carcinoma (relative risk, 24.342) and the Child-Pugh classification (relative risk, 5.780).
CONCLUSION. B-RTO is an effective method for gastric varices with gastrorenal shunt and provides lower recurrence and bleeding rates. We believe that B-RTO can become a standard treatment for gastric varices with gastrorenal shunt, although treatment of worsened esophageal varices may be necessary after B-RTO.
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In Japan, balloon-occluded retrograde transvenous obliteration (B-RTO) has been widely performed for gastric varices with gastrorenal shunt [3, 6, 10-15] since the safety and effectiveness of B-RTO were reported by Kanagawa et al. [16, 17]. Although B-RTO has become a common treatment of gastric varices in Japan and despite recent reports of its efficacy, it has not been widely adopted in other countries [3, 6, 10-15]. Most of the previous reports describe technical or short-term clinical results. Although there are two reports of the long-term clinical results after B-RTO [12, 13], a larger study is necessary to determine the long-term clinical efficacy. This uncontrolled, nonrandomized, retrospective cohort study was designed to evaluate the long-term clinical efficacy of B-RTO for gastric varices with gastrorenal shunt.
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The patient population included 47 men and 31 women (mean age, 62 ± [SD] 10 years; range, 34-80 years). The cause of their liver cirrhosis was hepatitis B (n = 6), hepatitis C (n = 48), chronic alcohol ingestion (n = 13), and others (n = 11). According to the Child-Pugh classification, 52 patients were categorized in class A, 24 patients in class B, and two patients in class C. The Child-Pugh score was 6.3 ± 1.3. Biochemical data before B-RTO revealed the following values: total bilirubin, 1.3 ± 0.9 (mg/dL); serum albumin, 3.3 ± 0.5 (g/dL); prothrombin time, 78 ± 22 (%); and ammonia, 87 ± 37 (µg/dL). Of the 78 patients, 24 had concomitant hepatocellular carcinoma (HCC) without portal tumor thrombus measuring less than 5 cm in diameter. Before the procedure, mild ascites was noted in two patients. None had severe ascites, and none had symptomatic hepatic coma.
All 78 patients had gastric varices with acute bleeding or danger of rupture. Gastric varices with a vascular diameter of over 5 mm on color Doppler endoscopic ultrasound and/or those with red spots on upper intestinal endoscopy were judged to be in danger of rupture [18]. The form of the varices was endoscopically evaluated according to the general rules proposed by the Japanese Research Society for Portal Hypertension [19]. The form of the varices was classified as small straight, enlarged tortuous, or large coil-shaped. The form of gastric varices was enlarged tortuous in 39 patients and large coil-shaped in the remaining 39 patients. Gastric varices were located in the fundus in 65 patients and in the cardia in the remaining 13 patients. Thirty-five patients had previous episodes of gastric variceal bleeding (urgent cases, n = 11; elective cases, n = 24), and the remaining 43 had no bleeding episodes of gastric varices (prophylactic cases, n = 43). Thirty-seven patients had both gastric varices and esophageal varices. The size of the esophageal varices was small straight in 27 patients and enlarged tortuous in 10 patients. Of the 37 patients with esophageal varices, seven had previous episodes of bleeding, and 11 had previous episodes of endoscopic injection sclerotherapy.
B-RTO Procedure
The B-RTO procedure is illustrated in Figures
1A,
1B,
1C,
1D, and
1E. A 6-French balloon catheter
with a diameter of 10 or 20 mm (MOIYAN, Miyano) was inserted into the
gastrorenal shunt via the right femoral vein. Through the balloon catheter,
retrograde venography was performed with the balloon inflated. If collateral
draining veins, such as an inferior phrenic vein, were visualized by
retrograde venography, they were embolized with microcoils to prevent leakage
of the sclerosing agent into the systemic circulation.
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When the gastric varices were visualized and retention of contrast medium in the gastric varices was identified, the sclerosing agent was slowly injected into the gastric varices from the balloon catheter until the feeding veins from the portal or splenic veins began to be visualized. After infusion of the sclerosing agent, the balloon was kept inflated overnight and the catheter was removed the next morning. The sclerosing agent was 5% ethanolamine oleate with iopamidol (Iopamiron, Schering) prepared by mixing equal volumes of 10% ethanolamine oleate (Oldamin, Takeda Pharmaceutical) and iopamidol. To prevent renal dysfunction caused by iopamidol-induced hemolysis, an IV drip infusion of 4,000 U of haptoglobin was given [3, 20].
Follow-Up Evaluation
Follow-up evaluation included recurrence and bleeding of gastric varices,
worsening of esophageal varices, and rate of survival. Gastrointestinal
endoscopy was routinely performed every 3-6 months after B-RTO. Endoscopic
findings for varices were evaluated by endoscopists according to the general
rules proposed by the Japanese Research Society for Portal Hypertension
[19]. In patients with a
bleeding episode after B-RTO, gastrointestinal endoscopy was immediately
performed to identify the site of bleeding. When endoscopy detected red spots
on esophageal varices and/or bleeding of esophageal varices, the esophageal
varices were judged to have worsened, and endoscopic injection sclerotherapy
was performed as soon as possible.
Definition of Follow-Up Period
The follow-up period in recurrence of gastric varices was measured in days
from the date of B-RTO until the first date when endoscopy revealed
morphologic recurrence of gastric varices or the date of the most recent
endoscopic examination. As for bleeding of gastric varices, the follow-up
period was calculated in days from the date of B-RTO until the date when
bleeding occurred or the date of the most recent clinical visit without a
bleeding episode.
The time to worsening of esophageal varices was calculated from the time of B-RTO to the date of endoscopic examination that showed worsening. If worsening of esophageal varices was not revealed by endoscopic examination, the follow-up period was measured from the date of B-RTO until the date of the most recent endoscopic examination.
The survival follow-up period was measured in days from the date of B-RTO until the date of death or most recent clinical visit. Patients without a visit during the most recent 6 months were investigated by telephone.
Statistical Analysis
All results were expressed as mean ± SD, median, or percentage. The
Kaplan-Meier method calculated the following cumulative rates: recurrence and
bleeding of gastric varices, worsening and bleeding of esophageal varices, and
rate of survival. Distributions of survival and time to worsening of
esophageal varices were analyzed in relation to each of the possible factors
(age, sex, location of gastric varices, form of gastric varices, previous
episode of bleeding of gastric varices, presence of esophageal varices,
presence of concomitant hepatocellular (HCC), and the Child-Pugh
classification). Univariate analyses (log-rank tests) were used to determine
differences in these distributions. Factors that seemed to have a significant
impact on time to worsening of esophageal varices or survival were entered
into Cox proportional hazards model to test for significant effects,
simultaneously adjusting for multiple factors. Significance was taken at a
p value of less than 0.05 for all tests. Statistical software
(Statview 5.0, SAS Institute) was used for statistical analyses.
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The median follow-up period in bleeding of gastric varices was 700 days (mean, 837 ± 533 days; range, 137-2,339 days). During the follow-up period, bleeding of gastric varices occurred in only one patient (1.3%) at 12 months after B-RTO. The patient had been noted to have recurrent gastric varices, and the bleeding occurred from the recurrence. The bleeding rate of gastric varices was 1.5% at 1 year, 1.5% at 3 years, and 1.5% at 5 years (Fig. 2B). In the other patient with recurrence of gastric varices, bleeding was not observed during the follow-up period.
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With respect to previous episode of bleeding of gastric varices, two (5.7%) of the 35 patients had gastric variceal recurrence and the recurrence rate was 6% at 1 year, 6% at 3 years, and 6% at 5 years. Rebleeding of gastric varices was observed in one (2.9%) of 35 patients; the rebleeding rate of gastric varices was 3.1% at 1 year, 3.1% at 3 years, and 3.1% at 5 years. In the 43 patients without previous episodes of bleeding, bleeding of gastric varices was not observed; the bleeding rate was 0% at 5 years.
Worsening of Esophageal Varices
During the follow-up period with a median of 368 days (mean, 493 ±
420 days; range, 37-1,954 days), esophageal varices worsened in 29 patients
(37%). The overall worsening rate of esophageal varices was 27% at 1 year, 58%
at 3 years, and 66% at 5 years (Fig.
3A). Bleeding of esophageal varices occurred in four patients
(5.1%) during the follow-up period with a median of 697 days (mean, 826
± 537 days; range, 137-2,339 days). The bleeding rate of esophageal
varices was 2.8% at 1 year, 4.3% at 3 years, and 9.1% at 5 years.
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In the univariate analysis, presence or absence of esophageal varices alone was a significant risk factor for worsening of esophageal varices after B-RTO (p < 0.01, Table 1). The worsening rates of esophageal varices at 1, 2, and 3 years were 35%, 66%, and 91% in the patients with esophageal varices and 21%, 21%, and 29% in the patients without them, respectively (p < 0.01, Fig. 3B). In the multivariate analysis, presence or absence of esophageal varices before B-RTO affected the time to worsening significantly (p < 0.01, Table 1). The patients with esophageal varices were likely to have a shorter time to worsening compared with the patients without them (relative risk, 4.956).
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To investigate more detailed risk factors in the 37 patients with esophageal varices, we performed univariate and multivariate analyses, using possible risk factors for esophageal varices (previous episodes of endoscopic injection sclerotherapy for esophageal variceal, previous episodes of esophageal variceal bleeding, and size of esophageal varices). However, significant detailed risk factors were not seen (Table 2).
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Survival
The median follow-up period in all 78 patients was 700 days (mean, 837
± 533 days; range, 137-2,339 days). During the follow-up period, 19
patients (24%) died. The median time to death was 686 days (mean, 791 ±
526 days; range, 137-1,987 days). The causes of death were hepatic failure
(n = 7), bleeding of gastric varices (n = 1), bleeding of
esophageal varices (n = 3), and HCC (n = 8). The overall
cumulative survival rates at 1, 3, and 5 years were 93%, 76% and 54%,
respectively (Fig. 4A).
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On the basis of univariate analysis, presence or absence of HCC and the Child-Pugh classification were significant prognostic factors related to survival (p < 0.05, Table 3). The survival rates at 1, 3, and 5 years were 83%, 60%, and 18% in the patients with HCC and 98%, 83%, and 30% in the patients without HCC, respectively (p < 0.01, Fig. 4B). In terms of the Child-Pugh classification, the survival rates at 1, 3, and 5 years were 94%, 87%, and 69% in class A; and 92%, 46%, and 16% in classes B and C, respectively (p < 0.05, Fig. 4C).
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In the multivariate and univariate analyses, presence or absence of HCC and the Child-Pugh classification were significant prognostic factors affecting survival after B-RTO (p < 0.01, Table 3). The multivariate analysis also showed that survival rate was significantly lower in the patients with HCC than in those without it (relative risk, 24.342) and significantly lower in patients whose condition was classified as Child-Pugh B and C than in those in class A (relative risk, 5.780). With respect to these prognosis-determining factors, survival rates were as follows: In the patients without HCC, the survival rates at 1, 3, and 5 years were 100%, 96%, and 96% in Child-Pugh class A; and 94%, 72%, and 19% in Child-Pugh classes B and C, respectively (p < 0.01). In the patients with HCC, there was no significant difference in the Child-Pugh classification.
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Shunt surgery is invasive and the operative mortality rate is 3-15% [23, 24]. Besides, for patients with poor liver function, reserve shunt surgery is usually contraindicated [25, 26]. Gastric varices with spontaneous gastrorenal shunt are usually difficult to treat by endoscopic injection sclerotherapy because the endoscopic approach is difficult and the intravariceal blood flow is too fast to permit injection of sufficient sclerosant [17, 27]. Kind et al. [28] have reported that the early rebleeding rate of gastric varices was 15.5% in 174 patients, which shows that endoscopic injection sclerotherapy is not the best treatment. In addition, endoscopic injection sclerotherapy for gastric varices could cause embolism of other organs due to a large gastrorenal shunt.
TIPS is a common decompression therapy for esophagogastric varices in America and Europe [23, 24, 29-31]. However, its reported effective rate for gastric varices is 50-63% and lower than that for esophageal varices [29, 32]. The reason may be that the portal pressure gradient is lower in patients who have gastric varices with spontaneous gastrorenal shunt, as reported by Watanabe et al. [1]; for TIPS, hepatic encephalopathy and shunt obstruction are severe problems.
Thus, an adequate treatment for gastric varices has not yet been established. Recently, B-RTO was reported as an effective new method. In fact, we have reported transcatheter sclerotherapy such as B-RTO may provide better control of bleeding of gastric varices than TIPS [33]. To establish a standard treatment for gastric varices, it is necessary to evaluate the long-term results in detail. This study shows the long-term results after B-RTO regarding recurrence and bleeding of gastric varices, worsening and bleeding of esophageal varices, and survival.
Reportedly, gastric varices thrombosed by B-RTO usually show marked shrinking and are completely resolved. The recurrence rate of gastric varices after B-RTO is reported as 0-10% [3, 6, 10-14, 16, 17], which is an excellent outcome. Our results were consistent with these reports. Despite the fact that bleeding of gastric varices after B-RTO was not usually reported, one patient in our study had bleeding. We propose that recurrent gastric varices need to be treated as soon as possible. Our study showed that the cumulative recurrence and bleeding rates of gastric varices at 5 years were 2.7% and 1.5%, respectively. We believe that B-RTO provides lower recurrence and bleeding rates than those of any other treatment and that B-RTO could become a standard treatment for gastric varices. The reader may claim that these outcomes are difficult to accept because this study includes many prophylactic cases. However, B-RTO actually provided a rebleeding rate as low as 3.1% at 5 years in the patients with previous episodes of bleeding of gastric varices. Moreover, in the patients without previous episodes of bleeding, the bleeding rate was 0% at 5 years. Kim et al. [18] have reported that the cumulative bleeding rates of gastric varices at 1, 3, and 5 years were 16%, 36%, and 44%, respectively. Therefore, we propose that it is clinically important to treat gastric varices in danger of rupture.
B-RTO can be expected to elevate the portal pressure gradient due to obstruction of a large gastrorenal shunt. Therefore, worsening of esophageal varices is one problem after B-RTO in long-term follow-up. Several reports show that the worsening rate of esophageal varices is 10-63% [3, 6, 12-14]. However, worsening of esophageal varices has not been evaluated in detail. In our study, the worsening rate in patients with esophageal varices was significantly higher than that in those without them. Moreover, multivariate analysis also showed that esophageal varices tended to worsen about five times more frequently in the patients with esophageal varices before B-RTO than in those without them. We think that those with worsened esophageal varices would bleed frequently when endoscopic injection sclerotherapy was not performed for them. However, because of endoscopic treatment, those patients with worsened esophageal varices were sufficiently controlled, although four patients did have bleeding of esophageal varices after B-RTO. We propose that endoscopic examination is extremely important for discovering worsening of esophageal varices after B-RTO and, in particular, endoscopic injection sclerotherapy is necessary and useful for preventing bleeding of worsened esophageal varices.
In terms of survival, prognostic factors are presence or absence of concomitant HCC and the Child-Pugh classification. Fukuda et al. [12] also reported the Child-Pugh classification as a prognostic factor related to survival. The outcome is the natural course of liver cirrhosis due to hepatitis virus. We propose that the value of B-RTO in survival is to reduce death due to bleeding of gastric varices. Actually, Kim et al. [18] have reported that most deaths occurred within 1 year after bleeding of gastric varices and that the cumulative survival at 1 year was 48% [18]. In addition, some reports indicate that B-RTO increases portal blood flow to the liver parenchyma and contributes to an improvement in liver function [10, 12, 34, 35]. We also have reported that liver function tended to improve in patients treated by transcatheter sclerotherapy such as B-RTO [33]. From the viewpoint of influencing liver function, B-RTO might contribute to increasing survival.
In conclusion, B-RTO is an effective method for gastric varices with gastrorenal shunt and provides lower recurrence and bleeding rates. We believe that B-RTO can become a standard treatment for gastric varices with gastrorenal shunt, although treatment of worsened esophageal varices, such as endoscopic injection sclerotherapy, may be necessary after B-RTO.
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