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DOI:10.2214/AJR.07.3356
AJR 2008; 191:555-559
© American Roentgen Ray Society


Original Research

Gastric Varices with Gastrorenal Shunt: Combined Therapy Using Transjugular Retrograde Obliteration and Partial Splenic Embolization

Fumio Chikamori1, Nobutoshi Kuniyoshi2, Takahiko Kawashima3 and Yasuhiro Takase3

1 Department of Surgery, Kuniyoshi Hospital, 1-3-4 Kamimachi, Kochi, Japan 780-0901.
2 Department of Internal Medicine, Kuniyoshi Hospital, Kochi, Japan.
3 Department of Surgery, Tsukuba Soai Hospital, Ibaraki, Japan.

Received October 26, 2007; accepted after revision February 23, 2008.

 
Address correspondence to F. Chikamori (chikamo1{at}i-kochi.or.jp).


Abstract
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
OBJECTIVE. This study was prospectively conducted to evaluate the effectiveness of the combination of transjugular retrograde obliteration and partial splenic embolization in the treatment of gastric varices with gastrorenal shunt.

SUBJECTS AND METHODS. Between November 2002 and December 2006, 14 patients with gastric varices and gastrorenal shunt were treated by combining transjugular retrograde obliteration and partial splenic embolization (group 1). These patients were compared with 19 patients with gastric varices and gastrorenal shunt treated by only transjugular retrograde obliteration (group 2) for the disappearance rate of gastric varices, the cumulative survival rate, and the occurrence rate of esophageal varices after transjugular retrograde obliteration. Partial splenic embolization was performed 7–14 days before transjugular retrograde obliteration. No significant differences were seen between the two groups in terms of demographic data, including age, sex, and Child-Pugh classification.

RESULTS. The disappearance rate of gastric varices after transjugular retrograde obliteration was 100% in both groups. The 3-year cumulative survival rate after transjugular retrograde obliteration was 92% in group 1 and 95% in group 2. The 3-year cumulative occurrence rate of esophageal varices after transjugular retrograde obliteration was 9% in group 1 and 45% in group 2, a significant difference (p < 0.05).

CONCLUSION. The findings of this study indicate that partial splenic embolization contributed to preventing portal congestion after transjugular retrograde obliteration. We conclude that the combination of transjugular retrograde obliteration and partial splenic embolization for gastric varices is more effective than transjugular retrograde obliteration only in the long-term prevention of esophageal varices after transjugular retrograde obliteration.

Keywords: gastric varices • gastrorenal shunt • partial splenic embolization • transjugular retrograde obliteration


Introduction
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Transvenous retrograde oblit eration has recently become the treatment of choice for gastric varices with a gastrorenal shunt in many institutions in Japan [1, 2]. The method of transvenous retrograde obliteration has two approaches: the transjugular and the trans femoral. The former is called transjugular retrograde obliteration [1] and the latter, balloon-occluded retrograde transvenous obliteration [2]. As we reported in a previous article [1], transjugular retrograde obliteration is less invasive and is effective in eradicating gastric varices. However, the high occurrence rate of esophageal varices after transjugular retrograde obliteration is still a problem [3]. Newly developed esophageal varices after transjugular retrograde obliteration can be easily treated with endoscopic injection sclerotherapy. However, the development of esophageal varices after trans jugular retrograde obliteration means a continuous pathologic state of portal circulation. Our previous study [4] showed that transjugular retrograde obliteration obliterates the gastrorenal shunt, which has an abundant blood flow, and increases portal venous pressure. Partial splenic embolization has the effect of decreasing splenic blood flow and portal venous pressure [5]. So we considered that partial splenic embolization may prevent the side effect of transjugular retrograde obliteration. This study was undertaken to evaluate the efficacy and safety of the combined treatment of transjugular retrograde obliteration and partial splenic embolization compared with transjugular retrograde obliteration only.


Subjects and Methods
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Patients
Thirty-three consecutive patients with portal hypertension, seen between November 2002 and December 2006, who had gastric varices and a gastrorenal shunt were included in this study if the size of the varices was more than F2 (mediumsized and nodular). Fourteen patients with liver cirrhosis were admit ted to our institution and treated by a combin ation of transjugular retrograde obliteration and partial splenic embolization (group 1). Nineteen patients with liver cirrhosis were admitted to an affiliated hospital and were treated by only transjugular retrograde obliteration (group 2). We analyzed the disappearance rate of gastric varices, the rate of complications, the cumulative survival rate, and the occurrence rate of esophageal varices after transjugular retrograde obliteration. Demographic data, including age, sex, and Child-Pugh classi fication for the two groups, are listed in Table 1. Our institutional review board approved this study, and informed consent was obtained from every patient.


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TABLE 1: Demographic Data of the Two Groups

 

No significant differences were seen between the two groups. In group 1, three patients had a history of gastric variceal bleeding and were treated electively, and 11 had no history of bleeding and were treated prophylactically. In group 2, three patients were treated electively and 16 patients prophylactically. Two patients in group 1 and two patients in group 2 had hepato cellular carcinoma smaller than 3 cm in diameter. We encountered complicated large gastroesophageal varices with a gastrorenal shunt in three and four patients in groups 1 and 2, respectively. In these cases, endoscopic injection sclerotherapy was nec essary before transjugular retrograde obliteration.


Figure 1
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Fig. 1A 40-year-old man with alcoholic cirrhosis was admitted for treatment of large gastric varices. Laboratory data on admission were as follows: WBC, 4,900/µL; hemoglobin, 13.3 g/dL; platelets, 8.6 x 104/µL; albumin, 2.6 g/dL; total bilirubin, 2.4 mg/dL; glutamic oxaloacetic transaminase, 59 U/L; glutamic pyruvic transaminase, 34 U/L; prothrombin time, 59.0%; hepaplastin test, 48%; total bile acid, 81.1 µmol/L; arterial ketone body ratio (AKBR), 0.3. Plasma ammonia level was 145 µg/dL, and indocyanine green retention rate at 15 min (ICG15) was 33%. Child-Pugh score was grade B. Antibodies to hepatitis B and C were negative. Patient was treated with partial splenic embolization and transjugular retrograde obliteration. Superior mesenteric arterial portography shows that gastric varices are supplied by left gastric vein and drained into gastrorenal shunt (arrow) and inferior phrenic vein.

 


Figure 2
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Fig. 1B 40-year-old man with alcoholic cirrhosis was admitted for treatment of large gastric varices. Laboratory data on admission were as follows: WBC, 4,900/µL; hemoglobin, 13.3 g/dL; platelets, 8.6 x 104/µL; albumin, 2.6 g/dL; total bilirubin, 2.4 mg/dL; glutamic oxaloacetic transaminase, 59 U/L; glutamic pyruvic transaminase, 34 U/L; prothrombin time, 59.0%; hepaplastin test, 48%; total bile acid, 81.1 µmol/L; arterial ketone body ratio (AKBR), 0.3. Plasma ammonia level was 145 µg/dL, and indocyanine green retention rate at 15 min (ICG15) was 33%. Child-Pugh score was grade B. Antibodies to hepatitis B and C were negative. Patient was treated with partial splenic embolization and transjugular retrograde obliteration. After microcoil obliteration of inferior phrenic vein, 10 mL of 5% ethanolamine oleate with iopamidol was injected into gastric varices (arrow), as shown on retrograde shunt venography.

 


Figure 3
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Fig. 1C 40-year-old man with alcoholic cirrhosis was admitted for treatment of large gastric varices. Laboratory data on admission were as follows: WBC, 4,900/µL; hemoglobin, 13.3 g/dL; platelets, 8.6 x 104/µL; albumin, 2.6 g/dL; total bilirubin, 2.4 mg/dL; glutamic oxaloacetic transaminase, 59 U/L; glutamic pyruvic transaminase, 34 U/L; prothrombin time, 59.0%; hepaplastin test, 48%; total bile acid, 81.1 µmol/L; arterial ketone body ratio (AKBR), 0.3. Plasma ammonia level was 145 µg/dL, and indocyanine green retention rate at 15 min (ICG15) was 33%. Child-Pugh score was grade B. Antibodies to hepatitis B and C were negative. Patient was treated with partial splenic embolization and transjugular retrograde obliteration. Retrograde shunt venography on day 1 after transjugular retrograde obliteration shows that thrombi have formed in gastric varices (arrow).

 
Methods
Gastrorenal shunt was diagnosed on CT and superior mesenteric arterial portography (Fig. 1A). Partial splenic embolization was performed 7–14 days before transjugular retrograde obliteration. Through the right femoral artery, a 5-French catheter was selectively advanced to the splenic artery. Through this catheter, a 3-French microcatheter was positioned in the peripheral splenic artery distal to the great pancreatic artery. After selective splenic arteriography, more than 70% splenic arterial embolization was performed using platinum microcoils or stainless steel coils under fluoroscopic guidance. The splenic infarction area was confirmed on CT performed 1 week after partial splenic embolization. Systemic antibiotic medication was started on the day of partial splenic embolization and continued for 1 week.

The transjugular retrograde obliteration technique and the skill level of both interventional radiologists were the same at our hospital and the affiliated hospital. The technical details of transjugular retrograde obliteration have prev iously been reported [1]. Through the right internal jugular vein, we inserted an 8-French long cobrashaped sheath into the left renal vein. We then inserted a 5- or 6-French angiographic catheter with an occlusive balloon 11 or 20 mm in diameter into the gastrorenal shunt through a previously inserted sheath. The balloon was inflated with 0.7–4.0 mL of diluted contrast medium to stop the blood flow in the shunt. The communicating routes of the gastrorenal shunt, such as the inferior phrenic and retroperitoneal veins, were obliterated with a microcoil when a 3-French microcatheter could be inserted into these veins or with absolute ethanol when the microcatheter could not be inserted. After the procedure, gastric variceal blood flow was completely controlled, and we injected 5–20 mL of 5% ethanolamine oleate with iopamidol (EOI) into the gastric varices under fluoroscopic guidance (Fig. 1B). After confirming the presence of thrombi in the gastric varices on retrograde shunt venography the next day, we removed the catheter (Fig. 1C). If retrograde shunt venography revealed no thrombi in the varices, we repeated the procedure. The catheter was left in the vein for 1 or more days, depending on how rapidly thrombi formed in the gastric varices [3].

The success of obliteration of the gastric varices was confirmed on contrast-enhanced CT 1 week, 1 month, and 3 months after transjugular retrograde obliteration. Eradication of the gastric varices was diagnosed by endoscopic examination 1 week, 1 month, and 3 months after transjugular retrograde obliteration. After eradication of the gastric varices, follow-up by endoscopy and CT was performed every 6 months. Form of gastric or esophageal varices was classified into three types—F1, small and tortuous; F2, medium-sized and nodular; and F3, large and tumorous—and evaluated. Esophageal varices with the "red color" sign [6] that occurred after transjugular retrograde obliteration were treated with endo scopic injection sclerotherapy.

Statistical analysis was performed using Stat-View statistical software (Abacus Concepts, Inc.). The clinical data were tested using the Student's t test and the chi-square test. Survival curves were obtained by the Kaplan-Meier method. Analysis of survival curves for significance was performed using the log-rank test. Data were considered significant when the p value was less than 0.05. The results are given as mean ± SD.


Results
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
The success rate of gastric variceal eradication by transjugular retrograde oblit eration was 100% in both groups. Eighty-six percent (12/14) of gastric varices completely thrombosed on day 1 after transjugular retrograde obliteration in group 1 and 79% (15/19), in group 2. In the remaining two patients in group 1, the gastric varices were completely thrombosed on day 2. In group 2, the varices were completely thrombosed on day 2 in three patients and on day 3 in one. Major and minor complications for the two groups are listed in Table 2. Mild to moderate abdominal pain necessitating analgesic drugs was found in 100% (14/14) of the patients in group 1 and in 63% (12/19) of those in group 2, with a significant difference (p = 0.011). In group 2, one patient had worsening ascites and one had worsening portal hypertensive gastropathy necessitating medication. No significant differences were seen between the two groups in minor complications, including fever of more than 38°C, hematuria, and a small amount of pleural effusion. Form changes in gastric varices in both groups after transjugular retrograde obliteration are listed in Table 3. One hundred percent (14/14) of gastric varices in group 1 and 95% (18/19) in group 2 were markedly reduced in size 1 month after transjugular retrograde obliteration. The varices dis appeared 3 months after transjugular retrograde obliteration in both groups.


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TABLE 2: Comparison of Clinical Results of the Two Groups

 

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TABLE 3: Form of Changes of Gastric Varices After Transjugular Retrograde Obliteration in the Two Groups

 


Figure 4
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Fig. 2 Graph shows cumulative occurrence rate of esophageal varices after transjugular retrograde obliteration in groups 1 and 2. Lower line represents group 1, partial splenic embolization and transjugular retrograde obliteration; upper line, group 2, trans jugular retrograde obliteration only. Difference between the two groups was statistically significant (p < 0.05).

 
The 3-year cumulative survival rate after transjugular retrograde obliteration was 92% in group 1 and 95% in group 2. The 3-year recurrence rate of gastric varices after transjugular retrograde obliteration was 0% in both groups. The cumulative occurrence rates of esophageal varices with the red color sign after transjugular retrograde obliteration in group 1 at 6 months and 1, 2, and 3 years were 0%, 0%, 9%, and 9%, respectively, as opposed to 16%, 27%, 45%, and 45% in group 2 (Fig. 2). The differences between the two groups were statistically significant (p = 0.045). Endoscopic findings of these varices are listed in Table 4. Varices were treated with endoscopic injection sclerotherapy. Gastrointestinal bleeding was not observed after transjugular retrograde obliteration in either group. One patient in group 1 and one patient in group 2 died of liver failure 5 and 6 months, respectively, after transjugular retrograde obliteration.


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TABLE 4: Endoscopic Findings of Esophageal Varices Occurring After Transjugular Retrograde Obliteration in the Two Groups

 


Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
There is no standard treatment for gastric varices [710]. In patients with preserved liver function, periesophagogastric devascular ization and splenectomy—the Hassab procedure [11]—may be indicated. However, in patients with poor liver function this surgical approach is usually less well tolerated so that a minimally invasive alternative is warranted. A transjugular intrahepatic portosystemic shunt (TIPS) [12] can lower the portal venous pressure and may be indicated in patients with bleeding esophageal varices. However, the portal venous pressure in patients with gastric varices is usually lower than in patients with esophageal varices [13, 14].

We have been treating gastric varices using transjugular retrograde obliteration since September 1991 [1]. With our method, the sclerosant volume can be kept at a safe dose, unlike other methods [2]. There was no recurrence and no bleeding of gastric varices in any patient after transjugular retrograde obliteration. The overall cumulative survival rates after transjugular retrograde obliteration at 1, 3, and 5 years were 92%, 76%, and 61%, respectively [3]. Ninoi et al. [15] reported that the cumulative gastric variceal bleeding rate at 1 year was 20% in a TIPS group and 2% in a transvenous obliteration group (p < 0.01). The cumulative survival rates in the TIPS group at 1, 3, and 5 years were 81%, 64%, and 40%, respectively, as opposed to 96%, 83%, and 76% in the transvenous obliteration group, respectively (p < 0.01) [15]. On the basis of these results, TIPS cannot be recommended for the treatment of gastric varices.

Although transjugular retrograde obliteration has a dramatic effect in eradicating large gastric varices, it is weak for increasing portal venous pressure [4] and for accelerating the occurrence of esophageal varices in Child-Pugh classification B and C patients in the long term [3]. Flow in the paraesophageal vein and the trunk of the left gastric vein is not controlled by transjugular retrograde obliteration, and these vessels cannot be obliterated. Therefore, it is not surprising that esophageal varices occur through the left gastric vein or the cardiac venous plexus after transjugular retrograde obliteration. Even if esophageal varices after transjugular retrograde obliteration can be easily controlled by endoscopic injection sclero therapy before they bleed, the occurrence of esophageal varices after obliteration is a disadvantage to patients. Because the portal venous pressure in patients with gastric varices and a gastrorenal shunt is lower than in patients with esophageal varices, gastric varices may play a protective role in the development of esophageal varices. The issue is how to prevent the development of esophageal varices after the treatment of gastric varices by transjugular retrograde obliteration.

Many reports have revealed that partial splenic embolization effectively improves hypersplenism [16], portal hypertensive gastropathy [17], liver function [18], and the prognosis of patients who have undergone endoscopic injection sclerotherapy for esophageal varices [19]. Our results confirm that partial splenic embolization can reduce the hyperdynamic cycle of portal hypertension and, in combination with transjugular retrograde obliteration, decrease the occurrence rate of esophageal varices. We believe that partial splenic embolization contributed to preventing the increase of portal venous pres sure after transjugular retrograde obliteration. We further believe that partial splenic embolization has the potential to compensate for the drawbacks of transjugular retrograde obliteration; we will be using this combination therapy for gastric varices in future patients. In this study, we performed partial splenic embolization and transjugular retrograde obliteration on separate days because the access routes of the two procedures are different. The procedures can also be performed on the same day, thereby saving the patient a trip to interventional radiology.

On the other hand, some patients have complicated gastroesophageal varices with a gastrorenal shunt. Such cases are less common than isolated gastric varices and are thought to be in a serious stage of portal hypertension [20]. In these cases, endoscopic injection sclerotherapy is necessary before transjugular retrograde obliteration. Because endoscopic injection sclerotherapy and transjugular retrograde obliteration bring further congestion in the portal venous system, partial splenic embolization is strongly recommended. Randomized controlled trials are also needed to evaluate whether the combined treatment of transjugular retrograde obliteration and partial splenic embolization is more effective than the devascularization proposed by Hassab [11]. We conclude that the combination of transjugular retrograde obliteration and partial splenic embolization for gastric varices is more effective than transjugular retrograde obliteration alone in the long-term prevention of esophageal varices after transjugular retrograde obliteration.


References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 

  1. Chikamori F, Shibuya S, Takase Y, Ozaki A, Fukao K. Transjugular retrograde obliteration for gastric varices. Abdom Imaging 1996; 21:299 -303[CrossRef][Medline]
  2. Kanagawa H, Mima S, Kouyama H, Gotoh K, Uchida T, Okuda K. Treatment of gastric fundal varices by balloon-occluded retrograde obliteration. Gastroenterol Hepatol 1996;11 : 51-58[CrossRef]
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  4. Chikamori F, Kuniyoshi N, Shibuya S, Takase Y. Short-term portal hemodynamic effects of transjugular retrograde obliteration of gastric varices with gastrorenal shunts. Dig Surg 2000;17 : 332-336[CrossRef][Medline]
  5. Chikamori F, Kuniyoshi N, Shibuya S, Takase Y. Short-term portal hemodynamic effects of partial splenic embolization for hypersplenism. Hepatogastroenterology 2007;54 : 1847-1849[Medline]
  6. Beppu K, Iniokuchi K, Koyanagi N, et al. Prediction of variceal hemorrhage by esophageal endoscopy. Gastrointest Endosc 1981; 27:213 -218[Medline]
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  8. Ramond MJ, Valla D, Mosnier JF, et al. Successful endoscopic obturation of gastric varices with butyl cyanoacrylate. Hepatology 1989;10 : 488-493[CrossRef][Medline]
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  11. Hassab MA. Gastroesophageal decongestion and splenectomy in the treatment of esophageal varices in bilharzial cirrhosis: further studies with a report of 355 operations. Surgery 1967;61 : 169-17.[Medline]
  12. LaBerge JM, Ring EJ, Gordon RL, et al. Creation of transjugular intrahepatic portosystemic shunts with the Wallstent endoprosthesis: results in 100 patients. Radiology 1993;187 : 413-420[Abstract/Free Full Text]
  13. Chikamori F, Kuniyoshi N, Shibuya S, Takase Y. Correlation between endoscopic and angiographic findings in patients with esophageal and isolated gastric varices. Dig Surg 2001;18 : 176-181[CrossRef][Medline]
  14. Watanabe K, Kimura K, Matsutani S, Ohto M, Okuda K. Portal hemodynamics in patients with gastric varices: a study in 230 patients with esophageal and/or gastric varices using portal vein catheterization. Gastroenterology 1988;95 : 434-440[Medline]
  15. Ninoi T, Nakamura K, Kaminou T, et al. TIPS versus transcatheter sclerotherapy for gastric varices. AJR2004; 183:369 -376[Abstract/Free Full Text]
  16. Owman T, Lunderquist A, Alwmark A, Borjesson B. Embolization of the spleen for treatment of splenomegaly and hypersplenism in patients with portal hypertension. Invest Radiol 1979;14 : 457-464[Medline]
  17. Shimizu T, Onda M, Tajiri T, et al. Bleeding portal-hypertensive gastropathy managed successfully by partial splenic embolization. Hepatogastroenterology 2002;49 : 947-949[Medline]
  18. Tajiri T, Onda M, Yoshida H, Mamada Y, Taniai N, Kumazaki T. Long-term hematological and biochemical effects of partial splenic embolization in hepatic cirrhosis. Hepatogastroenterology 2002;49 : 1445-1448[Medline]
  19. Tajiri T, Onda M, Taniai N, Yoshida H, Mamada Y. A comparison of combination endoscopic therapy and interventional radiology with esophageal transection for the treatment of esophageal varices. Hepatogastroenterology 2002;49 : 1552-1554[Medline]
  20. Chikamori F, Kuniyoshi N, Kawashima T, Shibuya S, Takase Y. Combination treatment of partial splenic embolization, endoscopic embolization and transjugular retrograde obliteration for complicated gastroesophageal varices. Hepatogastroenterology 2004;51 : 1506-1509[Medline]

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