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Balloon-Occluded Retrograde Transvenous Obliteration of Gastric Varices from Unconventional Systemic Veins in the Absence of Gastrorenal Shunts
Balloon-Occluded Retrograde Transvenous Obliteration of Gastric Varices from Unconventional Systemic Veins in the Absence of Gastrorenal Shunts Takuji Araki, MD,* and Wael E.A. Saad, MD, FSIR† Balloon-occluded retrograde transvenous obliteration of gastric varices in the absence of a gastrorenal shunts can still be performed through unconventional venous routes, such as the left inferior phrenic (ascending portion or transverse portion), pericardial, and azygoushemiazygous veins. This requires detailed knowledge of venous anatomy, impeccable preprocedural imaging for planning, and high-skill set techniques with smaller balloonocclusion catheters. The technical results appear to be high (67%-83% depending on the access venous system available), but are lower than conventional balloon-occluded retrograde transvenous obliteration via the gastrorenal shunt. Tech Vasc Interventional Rad 15:241-253 © 2012 Elsevier Inc. All rights reserved. KEYWORDS BRTO, transvenous obliteration, varices, unconventional
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emodynamic studies of gastric varices have revealed several types of draining pathways from these varices (Fig. 1).1-4 Balloon-occluded retrograde transvenous obliteration (BRTO) for gastric varices at the gastric fundus can be performed through a gastrorenal shunt, which is a large and common draining pathway from the descending part of the left inferior phrenic vein connecting with the left adrenal vein. The descending part of the left inferior phrenic vein has some anastomoses with small gastric veins, which can provide entrance into the systemic venous system from the gastric veins of the portal venous system.2,4 However, approximately 15% patients with gastric varices do not have a gastrorenal shunt account as a main draining vein.4,5 In such cases, various other portosystemic venous pathways may provide the main draining route.2,4,6 One of these portosystemic venous pathways involves the transverse part of the inferior phrenic vein, which passes under the diaphragm and connects directly with the inferior vena cava (IVC).4-9 Other venous drainage routes can be via the pericardial vein to the left brachiocephalic vein. An additional pathway is the paraesophageal vein—a draining pathway to the azygos ve-
*Department of Radiology, University of Yamanashi, University Hospital, Yamanashi, Japan. †Department of Radiology and Medical Imaging, Vascular & Interventional Radiology Division, University of Virginia Health System, Charlottesville, VA. Address reprint requests to: Takuji Araki, MD, Department of Radiology, University of Yamanashi, University Hospital, 1110 Shimokato Chuo, Yamanashi 409-3898, Japan. E-mail: [email protected] 1089-2516/12/$-see front matter © 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.tvir.2012.07.006
nous system that may develop in gastric varices at the cardiac ring.6,9 The article discusses the anatomy, techniques, and results of BRTO of gastric varices via these less common portosystemic venous routes that drain isolated gastric varices. The outline of what is discussed in this article in the broader scheme of transvenous obliteration of gastric varices is demonstrated in Fig. 2.
Anatomy and Technique The Left Inferior Phrenic Vein System The left inferior phrenic vein system is composed of the left inferior phrenic vein(s) and its components and the left pericardial vein (Figs. 1 and 3). The left inferior phrenic vein is composed of a transverse part and a vertical part (Figs. 1 and 3). The vertical part of the left inferior phrenic vein is composed of an ascending part and a descending part (Figs. 1 and 3) from the anastomosis with gastric veins. It is this descending part that anastomoses with the left adrenal vein to form the gastrorenal shunt (Figs. 1 and 3).
The transverse part of the left inferior phrenic vein The transverse part of the left inferior phrenic vein can be a main draining vein from isolated gastric varices of the fundus and occur at a frequency of 10%-15% (Fig. 4A-F).7,9 The 241
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Figure 1 An illustration of the venous anatomy around gastric varices without a gastrorenal shunt. Rt BCV, right brachiocephalic vein; Lt BCV, left brachiocephalic vein; Lt SV, left subclavian vein; SVC, superior vena cava; IVC, inferior vena cava; E, esophagus; SV, splenic vein; MV, mesenteric vein(s); PV, portal vein; Peric V, pericardial vein; TpIPV, transverse portion of the inferior phrenic vein; ApIPV, ascending part of the vertical portion of the inferior phrenic vein. The descending part of the vertical portion of the inferior phrenic vein is believed to form the gastrorenal shunt by anastomosing with the adrenal vein. GV, Gastric varices/varix; LGV, left gastric vein (coronary vein).
inferior phrenic vein has two potential outlets: the left adrenal vein and IVC. However, venograms of the left inferior phrenic vein in patients with normal liver function do not always show its entirety, and the left inferior phrenic vein often has separated pathways into different outlets (Fig. 5). Because of the incomplete course of the left inferior phrenic vein, a main draining vein from the transverse part of the left inferior phrenic vein occasionally is present. Enhanced computed tomography (CT) scans demonstrate this route under the diaphragm (Fig. 4B) without the gastrorenal shunt connecting the left renal vein. CT during splenic arteriography is useful to confirm the presence of the main draining vein. The outlet of this route is directly the IVC or the root of the left hepatic vein (Fig. 4D). For BRTO via this route, a curved long sheath should be inserted into the transverse portion to make manipulation of the balloon-occlusion catheter easier. The transverse part of the left inferior phrenic vein has a sharp turn at the left diaphragm from the transverse portion to the ascending portion (Figs. 1, 4A, 6). A balloon catheter should be introduced near the gastric varices beyond the sharp turn. In cases where the angle of the turn is too acute,
a 3.5-French balloon-occlusion catheter may be useful. When the ascending portion divides into two routes, the balloon-occlusion catheter should be passed beyond the bifurcation point of the ascending portion (Figs. 4Aii and 6). When the balloon-occlusion catheter cannot be introduced beyond the sharp-angled turn (dashed arrow, Fig. 6), it is necessary to embolize or pass beyond several collateral draining veins, such as the pericardial vein or anastomosis with the intercostal or retroperitoneal veins to completely retrograde fill the ascending portion with contrast materials for venograph or sclerosing agents for transvenous obliteration treatment. Special attention during BRTO should be given to the existence of a portopulmonary venous anastomosis, which can cause a paradoxical embolism like cerebral infarction by sclerosing agents or clots outflowing escaping via this anastomosis into the systemic circulation.10 The success rate of this procedure is almost the same or only slightly lower than that of conventional BRTO (in our experience, e: 83%).6
The pericardial vein (Fig. 7A-F) The pericardial vein, which is also described as the pericardiophrenic vein, connects the transverse part of the left infe-
BRTO from unconventional systemic veins in the absence of gastric shunts
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Figure 2 Flow chart demonstrating the technical approaches to variceal transvenous obliteration and highlighting the article’s discussion lineage, which is BRTO via unconventional systemic veins.
rior phrenic vein at the left diaphragm crossing the left border of the heart (Figs. 1 and 7A). This vein, which sometimes forms a common trunk with the left internal thoracic vein, flows out into the left brachiocephalic vein as it is or close to its transition to the left subclavian vein. The pericardial vein only infrequently develops as a main draining vein. However, the ascending part of the left inferior phrenic vein is present as a continuum with the pericardial vein, and the transverse part of the left inferior phrenic vein usually becomes a lesser collateral draining vein. Contrast-enhanced CT scans show the pericardial vein as a small vein on the left edge of the heart. The left jugular approach is needed to locate the outlet of the pericardial vein in the left brachiocephalic vein. This pathway is so long that insertion of a long sheath is required for handling of catheters or guide wires (Fig. 7A). The pathway from the pericardial vein to the transverse part of the left inferior phrenic vein often takes the form of a sharp turn and advancement of a guide wire or a balloon-occlusion catheter beyond the turn may be difficult. A 3.5-French balloon-occlusion catheter or multicoaxial system can be useful in these cases. When the balloon-occlusion catheter is introduced into the ascending part of the left inferior phrenic vein beyond the turn, BRTO can be performed in the same way as conventional BRTO (Fig. 7F). The approach for the pericardial vein is less difficult, but this route is longer and thinner than that via the transverse part of the left inferior phrenic vein. The length and thinness of this pathway and the sharp-
ness of the turn make this procedure more difficult. Extravasation may sometimes occur because of the thinness, but there are generally no critical complications associated with this extravasation. Nevertheless, the success rate of BRTO via the pericardial vein may be lower than that via the transverse part of the left inferior phrenic vein (in our experience, 2⁄3: 67%).6 In some case, double balloon occlusion from both the transverse part of the left inferior phrenic and pericardial veins may be required (Fig. 8).
The paraesophageal vein via the azygos vein Gastric varices at the cardiac ring (gastric cardia) are regarded as an intragastrically projected cardiac venous plexus, which connects to esophageal veins or paraesophageal veins (Fig. 9A-F). In isolated gastric varices at the cardiac ring on endoscopy, a large paraesophageal vein may be the main draining vein from the gastric varices apart from esophageal varices. However, the azygos venous system with a confluence of the esophageal, paraesophageal, intercostal, or mediastinal veins forms an extremely complicated venous network, and the outlet of the draining vein is usually difficult to identify on venography. The azygos venography under temporary balloon occlusion may demonstrate that the contrast materials flow out downstream through the venous network instead of providing retrograde enhancement of the branches. Cases with a paraesophageal vein can potentially be treated by
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Figure 3 An illustration of the venous anatomy around gastric varices without a gastrorenal shunt and the various unconventional systemic (BRTO) approaches to these gastric varices. A is the labeled version. B and C are the approaches via the transverse part of the inferior phrenic approach (unconventional subdiaphragmatic approach). In B, the balloon-occlusion catheter is advanced deeper beyond the transverse portion of the inferior phrenic vein and into the ascending part of the vertical portion of the inferior phrenic vein. D and E are the approaches transgressing the left hemidiaphragm (supradiaphragmatic approaches) from the pericardial vein (D) and the Azygous/Hemiazygous system (E). Rt BCV, right brachiocephalic vein; Lt BCV, left brachiocephalic vein; Lt SV, left subclavian vein; SVC, superior vena cava; IVC, inferior vena cava; E, esophagus; SV, splenic vein; MV, mesenteric vein(s); PV, portal vein; Peric V, pericardial vein; TpIPV, transverse portion of the inferior phrenic vein; ApIPV, ascending part of the vertical portion of the inferior phrenic vein. The descending part of the vertical portion of the inferior phrenic vein is believed to form the gastrorenal shunt by anastomosing with the adrenal vein. GV, Gastric varices/varix; LGV, left gastric vein (coronary vein).
BRTO from unconventional systemic veins in the absence of gastric shunts
Figure 4 A man in his 50s with a main draining pathway from the transverse part of the left inferior phrenic vein into the inferior vena cava. (A) An anatomical illustration of BRTO from the transverse part of the inferior phrenic vein. In Aii, the balloon-occlusion catheter is advanced deeper beyond the transverse portion of the inferior phrenic vein and into the ascending part of the vertical portion of the inferior phrenic vein. In Aiii, the balloon-occlusion catheter is still within the transverse portion of the inferior phrenic vein. Rt BCV, right brachiocephalic vein; Lt BCV, left brachiocephalic vein; Lt SV, left subclavian vein; SVC, superior vena cava; IVC, inferior vena cava; E, esophagus; SV, splenic vein; MV, mesenteric vein(s); PV, portal vein; Peric V, pericardial vein; TpIPV, transverse portion of the inferior phrenic vein; ApIPV, ascending part of the vertical portion of the inferior phrenic vein. The descending part of the vertical portion of the inferior phrenic vein is believed to form the gastrorenal shunt by anastomosing with the adrenal vein. GV, Gastric varices/varix; LGV, left gastric vein (coronary vein).
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Figure 4 (Continued) (B) Contrast-enhanced CT revealed a large draining vein from the gastric varices to the IVC, which was suggested to be the main draining pathway of the transverse portion of the inferior phrenic vein (black arrows). Ao, Aorta. (C) Splenic arteriography revealed GV with the transverse part (between solid black arrows) of the left inferior phrenic vein as the main draining vein. Leading to the transverse portion of the left inferior phrenic vein is the ascending portion of the left inferior phrenic vein (between solid white arrows). SpV, splenic vein; MPV, main portal vein. (D) An outlet of the draining left inferior phrenic vein was found to be the IVC as depicted by the contrast-enhanced CT (B). The selective catheter is seen in the IVC and is selecting the transverse portion of the left inferior phrenic vein (between solid arrows). (E) Balloon-occluded retrograde transvenous venography, which was performed at the root of the transverse part of the left inferior phrenic vein (hollow arrow at balloon site), demonstrated the main draining pathway (between solid white arrows, which is the ascending portion of the left inferior phrenic vein) with small collateral retroperitoneal draining veins (dashed arrows). The balloon occlusion catheter has been advanced from the inferior vena cava and through the transverse portion of the left inferior phrenic vein (between solid black arrows). (F) The balloon-occlusion catheter was inserted beyond the turn forming the transverse portion (between solid black arrows) to the ascending portion (between solid white arrows) to perform the balloon-occluded transvenous obliteration (BRTO) of the GV. The balloon-occlusion catheter is being advanced through a curved sheath, which has been placed at the entrance in the inferior vena cava (hollow arrow at sheath tip).
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Figure 6 BRTV, which was performed at one of bifurcated ascending portions of the inferior phrenic vein to gastric varices in a male in his 50s, demonstrated that the ascending portion of the main draining pathway was fenestrated (multiple branch points). The balloon (hollow arrow) is placed at one of the bifurcated ascending portions from the transverse portion (between solid white arrows) of the left inferior phrenic vein. The dotted arrow shows the turn between another of the bifurcated ascending portions and the transverse portion. The solid black arrows point to a bifurcation of the vertically oriented ascending portion of the left inferior phrenic vein.
BRTO, but they have lower feasibility than cases with the inferior phrenic vein or pericardial vein. This technique should be considered a supporting technique for percutaneous transhepatic obliteration (balloon-occluded antegrade transvenous obliteration [BATO]) and other procedures.
Other veins There have not been any reports that other veins can develop as the main draining vein(s) of isolated gastric varices, although the intercostal vein seems to be a possible draining vein speculative. Meanwhile, some cases, including cases after subtotal gastrectomy, may have numerous innominate draining veins instead of a main known draining vein.6
Results Figure 5 (A) Venography of the left inferior phrenic vein in a male in his 50s with normal liver function showed the complete course of the vein in its entirety. The approach is from the left RV. The solid arrows point to the vertical portion of the inferior phrenic vein and the hollow arrow points to the transverse subdiaphragmatic portion of the inferior phrenic vein (the entire course of the inferior phrenic vein, vertical and transverse, is seen). (B) Venography of the left inferior phrenic vein in a male in his 60s with normal liver function showed that the left inferior phrenic vein is consisted of several veins and that there is no contiguous vein (compare with A).
14.5% (n ⫽ 11/76) of patients presenting with gastric varices were found not to have the typical gastrorenal shunt to perform the traditional BRTO procedure via the left renal gastrorenal approach.6 As a result, alternative systemic venous access routes were used to perform a BRTO procedure.6 Eighty-two percent (n ⫽ 9/11) of cases had identifiable systemic venous routes, and the remaining (18%, n ⫽ 2/11) had numerous innominate collaterals, such as retroperitoneal plexus of veins.6 Some authors consider these alternative veins to be difficult to access from the major systemic venous access veins (the IVC, left brachiocephalic vein, and superior vena cava, respectively).11 They occasionally require smaller balloons (3.5-French, ⬍6-mm) to occlude them.6,11 Intuitively, if these veins are small and difficult to cannulate, the risk of extravasation is theoretically higher.11 This particularly true with the pericardial vein.6 In addition, the BRTO procedures
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Figure 7 (A) An anatomical illustration of BRTO from the pericardial vein. The pericardial vein is catheterized from the left subclavian vein. The balloon descends down the pericardial vein from above the diaphragm and, if possible, crosses the pericardial vein anastomosis with the transverse portion of the inferior phrenic vein, below the diaphragm. Rt BCV, right brachiocephalic vein; Lt BCV, left brachiocephalic vein; Lt SV, left subclavian vein; SVC, superior vena cava; IVC, inferior vena cava; E, esophagus; SV, splenic vein; MV, mesenteric vein(s); PV, portal vein; Peric V, pericardial vein; TpIPV, transverse portion of the inferior phrenic vein. (B) The portal venous phase of a splenic arteriogram demonstrated that the dilated pericardial vein (solid white arrows) along the border of the heart was the main draining vein from the gastric varices. (C) Venography of the pericardial vein (solid black arrows along its course) demonstrated the whole entirety of the drainage outflowing into the LBCV, which then empties into the SVC and RA. The pericardial vein is seen originating from below the level of the diaphragm (dashed arrow at level of left hemidiaphragm). The selective catheter (hollow arrow) is placed from a left internal jugular vein approach.
BRTO from unconventional systemic veins in the absence of gastric shunts
Figure 7 (Continued) (D) Balloon-occluded retrograde transvenous venography at the pericardial vein (hollow arrows) showed the several collateral draining veins, including the transverse part of the left inferior phrenic vein (solid white arrow). The main draining route of the ascending part of the left inferior phrenic vein showed stagnation of contrast in a fluctuating manner (between black arrows). The dotted curved arrow denotes the drainage of the ascending portion of the left inferior phrenic vein to the GV. (E) Balloon-occluded retrograde transvenous venography at the part closer (hollow arrow) to the gastric varices of the pericardial vein demonstrated the ascending part of the left inferior phrenic vein from the gastric varices (between black arrows). The white arrows point to the transverse component of the left inferior phrenic vein. (F) Insertion of the balloon-occlusion catheter (hollow arrow) into the ascending part (between solid arrow and hollow arrow) of the left inferior phrenic vein close to the GV, which enabled BRTO to be performed.
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Figure 8 A woman in her 70s with main draining pathways of the pericardial and transverse part of the left inferior phrenic veins. (A) Venography of the pericardial vein (solid black arrows) demonstrated that the small pericardial vein was connected, at an acute angle, with the transverse part of the left inferior phrenic vein (solid white arrow). (B) Balloon-occluded retrograde transvenous venography of the transverse part (between solid white arrows) of the left inferior phrenic vein from the inferior vena cava slightly showed the main draining vein (between solid black arrows). (C) Double balloon-occluded (hollow arrow pointing to overlapping balloons) retrograde transvenous venography from both the pericardiac and transverse inferior phrenic veins demonstrated the gastric varices (solid black arrows).
BRTO from unconventional systemic veins in the absence of gastric shunts
Figure 9 A woman in her 60s with a main draining pathway of the paraesophageal vein into the azygos vein. (A) An anatomical illustration of BRTO for the paraesophageal vein in this case. Rt BCV, right brachiocephalic vein; Lt BCV, left brachiocephalic vein; Lt SV, left subclavian vein; SVC, superior vena cava; IVC, inferior vena cava; E, esophagus; SV, splenic vein; MV, mesenteric vein(s); PV, portal vein; Peric V, pericardial vein; TpIPV, transverse portion of the inferior phrenic vein. (B) Portal phase in a superior mesenteric angiogram showed the dilated left gastric vein (between white arrows) flowing into the paraesophageal vein and mostly supplying EV and gastric varices at the cardiac ring. PV, main portal vein. MV, mesenteric vein(s). (C) The approach to the azygos vein. A transfemoral catheter (solid black arrows) is seen advanced up the superior vena cava and selecting the azygous vein (Az). The hollow arrow points to the azygous arch orifice.
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Figure 9 (Continued) (D) Balloon-occluded retrograde transvenous venography at the azygos vein (hollow arrow at balloon) showed a complicated venous network. In the venous network, a branch connected with the varices showed a “to and fro” movement of the contrast material (solid white arrow). (E) Introduction of the balloon catheter into the “to and fro” branch resulted in the successful stagnation of the contrast materials and visualization of the gastric varices (hollow arrows). (F) Image after the injection of the sclerosing agents which remained in the varices.
BRTO from unconventional systemic veins in the absence of gastric shunts performed solely from these veins require smaller volumes of sclerosing agents compared with traditional BRTO via a gastrorenal shunt: 12 mL (usually ⬍20 mL) vs an average of 20-30 mL (usually ⬍40 mL), respectively.6,12-16 Araki et al had a 67% success rate in cannulating identifiable (pericardiac vein, left inferior phrenic veins, and azygous-hemiazygous veins) veins and succeeded in performing a BRTO of the gastric varices in the 67% of cases (all the cases that were cannulated).6 BRTO is more likely to be successful via the left inferior phrenic vein (transverse or ascending components) than via the pericardiac vein: 83% vs 67%, respectively.6 When considering all comers with gastric varices and without gastrorenal shunts, the intent-to-treat success rate (including innominate veins) of cannulation and subsequent BRTO was 55% (n ⫽ 6/11).6
Conclusions BRTO in the absence of gastrorenal shunts can still be performed via unconventional venous routes, such as the left inferior phrenic, pericardiac, and azygous-hemiazygous veins. This requires care knowledge of venous anatomy, impeccable preprocedural imaging for planning, and high-skill set techniques with smaller occlusion balloons. The technical results appear to be high (67%-83% depending on the access venous system available) but are lower than conventional BRTO via the gastrorenal shunt (technical success ⬎90%).
References 1. Johns TN, Evans BB: Collateral pathways in portal hypertension. Ann Surg 155:838-845, 1962 2. Watanabe K, Kimura K, Matsutani S, et al: Portal hemodynamics in patients with gastric varices. Gastroenterologist 95:434-440, 1988 3. Sarin SK, Lahoti D, Saxena SP, et al: Prevalence, classification, and natural history of gastric varices: A long-term follow up study in 568 portal hypertension patients. Hepatology 16:1343-1349, 1992
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4. Chikamori F, Kuniyoshi N, Shibuya S, et al: Correlation between endoscopic and angiographic findings in patients with esophageal and isolated gastric varices. Dig Surg 18:176-181, 2001 5. Koito K, Namieno T, Nagakawa T, et al: Balloon-occluded retrograde transvenous obliteration for gastric varices with gastrorenal or gastrocaval collaterals. AJR Am J Roentgenol 167:1317-1320, 1996 6. Araki T, Hori M, Motosugi U, et al: Can balloon-occluded retrograde transvenous obliteration be performed for gastric varices without gastrorenal shunts? J Vasc Interv Radiol 21:663-670, 2010 7. Kiyosue H, Mori H, Matsumoto S, et al: Transcatheter obliteration of gastric varices: Part 1. Anatomic classification. Radiographics 23:911920, 2003 8. Kiyosue H, Mori H, Matsumoto S, et al: Transcatheter obliteration of gastric varices: Part 2. Strategy and techniques based on hemodynamic features. Radiographics 23:921-937, 2003 9. Kameda N, Higuchi K, Shiba M, et al: Management of gastric fundal varices without gastro-renal shunts in 15 patients. World J Gastroenterol 21:448-453, 2008 10. Kumar A, Gonzalez G, Wilkinson L, et al: Computed tomography findings of spontaneous porto-pulmonary shunts in 3 patients with portal hypertension. J Thorac Imaging 25:70-74, 2010 11. Saad WEA, Sze DY: Variations of balloon-occluded retrograde transvenous obliteration (BRTO): Balloon-occluded antergrade transvenous obliteration (BATO) and alternative/adjunctive routes for BRTO. Semin Interv Radiol 28:314-324, 2011 12. Ninoi T, Nakamura K, Kaminou T, et al: TIPS versus transcatheter sclerotherapy for gastric varices. AJR Am J Roentgenol 183:369-376, 2004 13. Hong CH, Kim HJ, Park JH, et al: Treatment of patients with gastric variceal hemorrhage: Endoscopic N-Butyl-2Cyanoacrylate injection versus balloon-occluded retrograde transvenous obliteration. Hepatology 24:372-378, 2009 14. Yamagami T, Kato T, Hirota T, et al: Infusion of 50% glucose solution before injection of ethanolamine oleate during balloon-occluded retrograde transvenous obliteration. Radiology 51:334-338, 2007 15. Kitamoto M, Imamura M, Kamada K, et al: Balloon-occluded retrograde transvenous obliteration of gastric fundal varices with hemorrhage. AJR Am J Roentgenol 178:1167-1174, 2002 16. Choi YH, Yoon CJ, Park JH, et al: Balloon-occluded retrograde transvenous obliteration for gastric variceal bleeding: Its feasibility compared with transjugular intrahepatic portosystemic shunt. Korean J Radiol 4:109-116, 2003
H
emodynamic studies of gastric varices have revealed several types of draining pathways from these varices (Fig. 1).1-4 Balloon-occluded retrograde transvenous obliteration (BRTO) for gastric varices at the gastric fundus can be performed through a gastrorenal shunt, which is a large and common draining pathway from the descending part of the left inferior phrenic vein connecting with the left adrenal vein. The descending part of the left inferior phrenic vein has some anastomoses with small gastric veins, which can provide entrance into the systemic venous system from the gastric veins of the portal venous system.2,4 However, approximately 15% patients with gastric varices do not have a gastrorenal shunt account as a main draining vein.4,5 In such cases, various other portosystemic venous pathways may provide the main draining route.2,4,6 One of these portosystemic venous pathways involves the transverse part of the inferior phrenic vein, which passes under the diaphragm and connects directly with the inferior vena cava (IVC).4-9 Other venous drainage routes can be via the pericardial vein to the left brachiocephalic vein. An additional pathway is the paraesophageal vein—a draining pathway to the azygos ve-
*Department of Radiology, University of Yamanashi, University Hospital, Yamanashi, Japan. †Department of Radiology and Medical Imaging, Vascular & Interventional Radiology Division, University of Virginia Health System, Charlottesville, VA. Address reprint requests to: Takuji Araki, MD, Department of Radiology, University of Yamanashi, University Hospital, 1110 Shimokato Chuo, Yamanashi 409-3898, Japan. E-mail: [email protected] 1089-2516/12/$-see front matter © 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.tvir.2012.07.006
nous system that may develop in gastric varices at the cardiac ring.6,9 The article discusses the anatomy, techniques, and results of BRTO of gastric varices via these less common portosystemic venous routes that drain isolated gastric varices. The outline of what is discussed in this article in the broader scheme of transvenous obliteration of gastric varices is demonstrated in Fig. 2.
Anatomy and Technique The Left Inferior Phrenic Vein System The left inferior phrenic vein system is composed of the left inferior phrenic vein(s) and its components and the left pericardial vein (Figs. 1 and 3). The left inferior phrenic vein is composed of a transverse part and a vertical part (Figs. 1 and 3). The vertical part of the left inferior phrenic vein is composed of an ascending part and a descending part (Figs. 1 and 3) from the anastomosis with gastric veins. It is this descending part that anastomoses with the left adrenal vein to form the gastrorenal shunt (Figs. 1 and 3).
The transverse part of the left inferior phrenic vein The transverse part of the left inferior phrenic vein can be a main draining vein from isolated gastric varices of the fundus and occur at a frequency of 10%-15% (Fig. 4A-F).7,9 The 241
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Figure 1 An illustration of the venous anatomy around gastric varices without a gastrorenal shunt. Rt BCV, right brachiocephalic vein; Lt BCV, left brachiocephalic vein; Lt SV, left subclavian vein; SVC, superior vena cava; IVC, inferior vena cava; E, esophagus; SV, splenic vein; MV, mesenteric vein(s); PV, portal vein; Peric V, pericardial vein; TpIPV, transverse portion of the inferior phrenic vein; ApIPV, ascending part of the vertical portion of the inferior phrenic vein. The descending part of the vertical portion of the inferior phrenic vein is believed to form the gastrorenal shunt by anastomosing with the adrenal vein. GV, Gastric varices/varix; LGV, left gastric vein (coronary vein).
inferior phrenic vein has two potential outlets: the left adrenal vein and IVC. However, venograms of the left inferior phrenic vein in patients with normal liver function do not always show its entirety, and the left inferior phrenic vein often has separated pathways into different outlets (Fig. 5). Because of the incomplete course of the left inferior phrenic vein, a main draining vein from the transverse part of the left inferior phrenic vein occasionally is present. Enhanced computed tomography (CT) scans demonstrate this route under the diaphragm (Fig. 4B) without the gastrorenal shunt connecting the left renal vein. CT during splenic arteriography is useful to confirm the presence of the main draining vein. The outlet of this route is directly the IVC or the root of the left hepatic vein (Fig. 4D). For BRTO via this route, a curved long sheath should be inserted into the transverse portion to make manipulation of the balloon-occlusion catheter easier. The transverse part of the left inferior phrenic vein has a sharp turn at the left diaphragm from the transverse portion to the ascending portion (Figs. 1, 4A, 6). A balloon catheter should be introduced near the gastric varices beyond the sharp turn. In cases where the angle of the turn is too acute,
a 3.5-French balloon-occlusion catheter may be useful. When the ascending portion divides into two routes, the balloon-occlusion catheter should be passed beyond the bifurcation point of the ascending portion (Figs. 4Aii and 6). When the balloon-occlusion catheter cannot be introduced beyond the sharp-angled turn (dashed arrow, Fig. 6), it is necessary to embolize or pass beyond several collateral draining veins, such as the pericardial vein or anastomosis with the intercostal or retroperitoneal veins to completely retrograde fill the ascending portion with contrast materials for venograph or sclerosing agents for transvenous obliteration treatment. Special attention during BRTO should be given to the existence of a portopulmonary venous anastomosis, which can cause a paradoxical embolism like cerebral infarction by sclerosing agents or clots outflowing escaping via this anastomosis into the systemic circulation.10 The success rate of this procedure is almost the same or only slightly lower than that of conventional BRTO (in our experience, e: 83%).6
The pericardial vein (Fig. 7A-F) The pericardial vein, which is also described as the pericardiophrenic vein, connects the transverse part of the left infe-
BRTO from unconventional systemic veins in the absence of gastric shunts
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Figure 2 Flow chart demonstrating the technical approaches to variceal transvenous obliteration and highlighting the article’s discussion lineage, which is BRTO via unconventional systemic veins.
rior phrenic vein at the left diaphragm crossing the left border of the heart (Figs. 1 and 7A). This vein, which sometimes forms a common trunk with the left internal thoracic vein, flows out into the left brachiocephalic vein as it is or close to its transition to the left subclavian vein. The pericardial vein only infrequently develops as a main draining vein. However, the ascending part of the left inferior phrenic vein is present as a continuum with the pericardial vein, and the transverse part of the left inferior phrenic vein usually becomes a lesser collateral draining vein. Contrast-enhanced CT scans show the pericardial vein as a small vein on the left edge of the heart. The left jugular approach is needed to locate the outlet of the pericardial vein in the left brachiocephalic vein. This pathway is so long that insertion of a long sheath is required for handling of catheters or guide wires (Fig. 7A). The pathway from the pericardial vein to the transverse part of the left inferior phrenic vein often takes the form of a sharp turn and advancement of a guide wire or a balloon-occlusion catheter beyond the turn may be difficult. A 3.5-French balloon-occlusion catheter or multicoaxial system can be useful in these cases. When the balloon-occlusion catheter is introduced into the ascending part of the left inferior phrenic vein beyond the turn, BRTO can be performed in the same way as conventional BRTO (Fig. 7F). The approach for the pericardial vein is less difficult, but this route is longer and thinner than that via the transverse part of the left inferior phrenic vein. The length and thinness of this pathway and the sharp-
ness of the turn make this procedure more difficult. Extravasation may sometimes occur because of the thinness, but there are generally no critical complications associated with this extravasation. Nevertheless, the success rate of BRTO via the pericardial vein may be lower than that via the transverse part of the left inferior phrenic vein (in our experience, 2⁄3: 67%).6 In some case, double balloon occlusion from both the transverse part of the left inferior phrenic and pericardial veins may be required (Fig. 8).
The paraesophageal vein via the azygos vein Gastric varices at the cardiac ring (gastric cardia) are regarded as an intragastrically projected cardiac venous plexus, which connects to esophageal veins or paraesophageal veins (Fig. 9A-F). In isolated gastric varices at the cardiac ring on endoscopy, a large paraesophageal vein may be the main draining vein from the gastric varices apart from esophageal varices. However, the azygos venous system with a confluence of the esophageal, paraesophageal, intercostal, or mediastinal veins forms an extremely complicated venous network, and the outlet of the draining vein is usually difficult to identify on venography. The azygos venography under temporary balloon occlusion may demonstrate that the contrast materials flow out downstream through the venous network instead of providing retrograde enhancement of the branches. Cases with a paraesophageal vein can potentially be treated by
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Figure 3 An illustration of the venous anatomy around gastric varices without a gastrorenal shunt and the various unconventional systemic (BRTO) approaches to these gastric varices. A is the labeled version. B and C are the approaches via the transverse part of the inferior phrenic approach (unconventional subdiaphragmatic approach). In B, the balloon-occlusion catheter is advanced deeper beyond the transverse portion of the inferior phrenic vein and into the ascending part of the vertical portion of the inferior phrenic vein. D and E are the approaches transgressing the left hemidiaphragm (supradiaphragmatic approaches) from the pericardial vein (D) and the Azygous/Hemiazygous system (E). Rt BCV, right brachiocephalic vein; Lt BCV, left brachiocephalic vein; Lt SV, left subclavian vein; SVC, superior vena cava; IVC, inferior vena cava; E, esophagus; SV, splenic vein; MV, mesenteric vein(s); PV, portal vein; Peric V, pericardial vein; TpIPV, transverse portion of the inferior phrenic vein; ApIPV, ascending part of the vertical portion of the inferior phrenic vein. The descending part of the vertical portion of the inferior phrenic vein is believed to form the gastrorenal shunt by anastomosing with the adrenal vein. GV, Gastric varices/varix; LGV, left gastric vein (coronary vein).
BRTO from unconventional systemic veins in the absence of gastric shunts
Figure 4 A man in his 50s with a main draining pathway from the transverse part of the left inferior phrenic vein into the inferior vena cava. (A) An anatomical illustration of BRTO from the transverse part of the inferior phrenic vein. In Aii, the balloon-occlusion catheter is advanced deeper beyond the transverse portion of the inferior phrenic vein and into the ascending part of the vertical portion of the inferior phrenic vein. In Aiii, the balloon-occlusion catheter is still within the transverse portion of the inferior phrenic vein. Rt BCV, right brachiocephalic vein; Lt BCV, left brachiocephalic vein; Lt SV, left subclavian vein; SVC, superior vena cava; IVC, inferior vena cava; E, esophagus; SV, splenic vein; MV, mesenteric vein(s); PV, portal vein; Peric V, pericardial vein; TpIPV, transverse portion of the inferior phrenic vein; ApIPV, ascending part of the vertical portion of the inferior phrenic vein. The descending part of the vertical portion of the inferior phrenic vein is believed to form the gastrorenal shunt by anastomosing with the adrenal vein. GV, Gastric varices/varix; LGV, left gastric vein (coronary vein).
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Figure 4 (Continued) (B) Contrast-enhanced CT revealed a large draining vein from the gastric varices to the IVC, which was suggested to be the main draining pathway of the transverse portion of the inferior phrenic vein (black arrows). Ao, Aorta. (C) Splenic arteriography revealed GV with the transverse part (between solid black arrows) of the left inferior phrenic vein as the main draining vein. Leading to the transverse portion of the left inferior phrenic vein is the ascending portion of the left inferior phrenic vein (between solid white arrows). SpV, splenic vein; MPV, main portal vein. (D) An outlet of the draining left inferior phrenic vein was found to be the IVC as depicted by the contrast-enhanced CT (B). The selective catheter is seen in the IVC and is selecting the transverse portion of the left inferior phrenic vein (between solid arrows). (E) Balloon-occluded retrograde transvenous venography, which was performed at the root of the transverse part of the left inferior phrenic vein (hollow arrow at balloon site), demonstrated the main draining pathway (between solid white arrows, which is the ascending portion of the left inferior phrenic vein) with small collateral retroperitoneal draining veins (dashed arrows). The balloon occlusion catheter has been advanced from the inferior vena cava and through the transverse portion of the left inferior phrenic vein (between solid black arrows). (F) The balloon-occlusion catheter was inserted beyond the turn forming the transverse portion (between solid black arrows) to the ascending portion (between solid white arrows) to perform the balloon-occluded transvenous obliteration (BRTO) of the GV. The balloon-occlusion catheter is being advanced through a curved sheath, which has been placed at the entrance in the inferior vena cava (hollow arrow at sheath tip).
BRTO from unconventional systemic veins in the absence of gastric shunts
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Figure 6 BRTV, which was performed at one of bifurcated ascending portions of the inferior phrenic vein to gastric varices in a male in his 50s, demonstrated that the ascending portion of the main draining pathway was fenestrated (multiple branch points). The balloon (hollow arrow) is placed at one of the bifurcated ascending portions from the transverse portion (between solid white arrows) of the left inferior phrenic vein. The dotted arrow shows the turn between another of the bifurcated ascending portions and the transverse portion. The solid black arrows point to a bifurcation of the vertically oriented ascending portion of the left inferior phrenic vein.
BRTO, but they have lower feasibility than cases with the inferior phrenic vein or pericardial vein. This technique should be considered a supporting technique for percutaneous transhepatic obliteration (balloon-occluded antegrade transvenous obliteration [BATO]) and other procedures.
Other veins There have not been any reports that other veins can develop as the main draining vein(s) of isolated gastric varices, although the intercostal vein seems to be a possible draining vein speculative. Meanwhile, some cases, including cases after subtotal gastrectomy, may have numerous innominate draining veins instead of a main known draining vein.6
Results Figure 5 (A) Venography of the left inferior phrenic vein in a male in his 50s with normal liver function showed the complete course of the vein in its entirety. The approach is from the left RV. The solid arrows point to the vertical portion of the inferior phrenic vein and the hollow arrow points to the transverse subdiaphragmatic portion of the inferior phrenic vein (the entire course of the inferior phrenic vein, vertical and transverse, is seen). (B) Venography of the left inferior phrenic vein in a male in his 60s with normal liver function showed that the left inferior phrenic vein is consisted of several veins and that there is no contiguous vein (compare with A).
14.5% (n ⫽ 11/76) of patients presenting with gastric varices were found not to have the typical gastrorenal shunt to perform the traditional BRTO procedure via the left renal gastrorenal approach.6 As a result, alternative systemic venous access routes were used to perform a BRTO procedure.6 Eighty-two percent (n ⫽ 9/11) of cases had identifiable systemic venous routes, and the remaining (18%, n ⫽ 2/11) had numerous innominate collaterals, such as retroperitoneal plexus of veins.6 Some authors consider these alternative veins to be difficult to access from the major systemic venous access veins (the IVC, left brachiocephalic vein, and superior vena cava, respectively).11 They occasionally require smaller balloons (3.5-French, ⬍6-mm) to occlude them.6,11 Intuitively, if these veins are small and difficult to cannulate, the risk of extravasation is theoretically higher.11 This particularly true with the pericardial vein.6 In addition, the BRTO procedures
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Figure 7 (A) An anatomical illustration of BRTO from the pericardial vein. The pericardial vein is catheterized from the left subclavian vein. The balloon descends down the pericardial vein from above the diaphragm and, if possible, crosses the pericardial vein anastomosis with the transverse portion of the inferior phrenic vein, below the diaphragm. Rt BCV, right brachiocephalic vein; Lt BCV, left brachiocephalic vein; Lt SV, left subclavian vein; SVC, superior vena cava; IVC, inferior vena cava; E, esophagus; SV, splenic vein; MV, mesenteric vein(s); PV, portal vein; Peric V, pericardial vein; TpIPV, transverse portion of the inferior phrenic vein. (B) The portal venous phase of a splenic arteriogram demonstrated that the dilated pericardial vein (solid white arrows) along the border of the heart was the main draining vein from the gastric varices. (C) Venography of the pericardial vein (solid black arrows along its course) demonstrated the whole entirety of the drainage outflowing into the LBCV, which then empties into the SVC and RA. The pericardial vein is seen originating from below the level of the diaphragm (dashed arrow at level of left hemidiaphragm). The selective catheter (hollow arrow) is placed from a left internal jugular vein approach.
BRTO from unconventional systemic veins in the absence of gastric shunts
Figure 7 (Continued) (D) Balloon-occluded retrograde transvenous venography at the pericardial vein (hollow arrows) showed the several collateral draining veins, including the transverse part of the left inferior phrenic vein (solid white arrow). The main draining route of the ascending part of the left inferior phrenic vein showed stagnation of contrast in a fluctuating manner (between black arrows). The dotted curved arrow denotes the drainage of the ascending portion of the left inferior phrenic vein to the GV. (E) Balloon-occluded retrograde transvenous venography at the part closer (hollow arrow) to the gastric varices of the pericardial vein demonstrated the ascending part of the left inferior phrenic vein from the gastric varices (between black arrows). The white arrows point to the transverse component of the left inferior phrenic vein. (F) Insertion of the balloon-occlusion catheter (hollow arrow) into the ascending part (between solid arrow and hollow arrow) of the left inferior phrenic vein close to the GV, which enabled BRTO to be performed.
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Figure 8 A woman in her 70s with main draining pathways of the pericardial and transverse part of the left inferior phrenic veins. (A) Venography of the pericardial vein (solid black arrows) demonstrated that the small pericardial vein was connected, at an acute angle, with the transverse part of the left inferior phrenic vein (solid white arrow). (B) Balloon-occluded retrograde transvenous venography of the transverse part (between solid white arrows) of the left inferior phrenic vein from the inferior vena cava slightly showed the main draining vein (between solid black arrows). (C) Double balloon-occluded (hollow arrow pointing to overlapping balloons) retrograde transvenous venography from both the pericardiac and transverse inferior phrenic veins demonstrated the gastric varices (solid black arrows).
BRTO from unconventional systemic veins in the absence of gastric shunts
Figure 9 A woman in her 60s with a main draining pathway of the paraesophageal vein into the azygos vein. (A) An anatomical illustration of BRTO for the paraesophageal vein in this case. Rt BCV, right brachiocephalic vein; Lt BCV, left brachiocephalic vein; Lt SV, left subclavian vein; SVC, superior vena cava; IVC, inferior vena cava; E, esophagus; SV, splenic vein; MV, mesenteric vein(s); PV, portal vein; Peric V, pericardial vein; TpIPV, transverse portion of the inferior phrenic vein. (B) Portal phase in a superior mesenteric angiogram showed the dilated left gastric vein (between white arrows) flowing into the paraesophageal vein and mostly supplying EV and gastric varices at the cardiac ring. PV, main portal vein. MV, mesenteric vein(s). (C) The approach to the azygos vein. A transfemoral catheter (solid black arrows) is seen advanced up the superior vena cava and selecting the azygous vein (Az). The hollow arrow points to the azygous arch orifice.
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Figure 9 (Continued) (D) Balloon-occluded retrograde transvenous venography at the azygos vein (hollow arrow at balloon) showed a complicated venous network. In the venous network, a branch connected with the varices showed a “to and fro” movement of the contrast material (solid white arrow). (E) Introduction of the balloon catheter into the “to and fro” branch resulted in the successful stagnation of the contrast materials and visualization of the gastric varices (hollow arrows). (F) Image after the injection of the sclerosing agents which remained in the varices.
BRTO from unconventional systemic veins in the absence of gastric shunts performed solely from these veins require smaller volumes of sclerosing agents compared with traditional BRTO via a gastrorenal shunt: 12 mL (usually ⬍20 mL) vs an average of 20-30 mL (usually ⬍40 mL), respectively.6,12-16 Araki et al had a 67% success rate in cannulating identifiable (pericardiac vein, left inferior phrenic veins, and azygous-hemiazygous veins) veins and succeeded in performing a BRTO of the gastric varices in the 67% of cases (all the cases that were cannulated).6 BRTO is more likely to be successful via the left inferior phrenic vein (transverse or ascending components) than via the pericardiac vein: 83% vs 67%, respectively.6 When considering all comers with gastric varices and without gastrorenal shunts, the intent-to-treat success rate (including innominate veins) of cannulation and subsequent BRTO was 55% (n ⫽ 6/11).6
Conclusions BRTO in the absence of gastrorenal shunts can still be performed via unconventional venous routes, such as the left inferior phrenic, pericardiac, and azygous-hemiazygous veins. This requires care knowledge of venous anatomy, impeccable preprocedural imaging for planning, and high-skill set techniques with smaller occlusion balloons. The technical results appear to be high (67%-83% depending on the access venous system available) but are lower than conventional BRTO via the gastrorenal shunt (technical success ⬎90%).
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4. Chikamori F, Kuniyoshi N, Shibuya S, et al: Correlation between endoscopic and angiographic findings in patients with esophageal and isolated gastric varices. Dig Surg 18:176-181, 2001 5. Koito K, Namieno T, Nagakawa T, et al: Balloon-occluded retrograde transvenous obliteration for gastric varices with gastrorenal or gastrocaval collaterals. AJR Am J Roentgenol 167:1317-1320, 1996 6. Araki T, Hori M, Motosugi U, et al: Can balloon-occluded retrograde transvenous obliteration be performed for gastric varices without gastrorenal shunts? J Vasc Interv Radiol 21:663-670, 2010 7. Kiyosue H, Mori H, Matsumoto S, et al: Transcatheter obliteration of gastric varices: Part 1. Anatomic classification. Radiographics 23:911920, 2003 8. Kiyosue H, Mori H, Matsumoto S, et al: Transcatheter obliteration of gastric varices: Part 2. Strategy and techniques based on hemodynamic features. Radiographics 23:921-937, 2003 9. Kameda N, Higuchi K, Shiba M, et al: Management of gastric fundal varices without gastro-renal shunts in 15 patients. World J Gastroenterol 21:448-453, 2008 10. Kumar A, Gonzalez G, Wilkinson L, et al: Computed tomography findings of spontaneous porto-pulmonary shunts in 3 patients with portal hypertension. J Thorac Imaging 25:70-74, 2010 11. Saad WEA, Sze DY: Variations of balloon-occluded retrograde transvenous obliteration (BRTO): Balloon-occluded antergrade transvenous obliteration (BATO) and alternative/adjunctive routes for BRTO. Semin Interv Radiol 28:314-324, 2011 12. Ninoi T, Nakamura K, Kaminou T, et al: TIPS versus transcatheter sclerotherapy for gastric varices. AJR Am J Roentgenol 183:369-376, 2004 13. Hong CH, Kim HJ, Park JH, et al: Treatment of patients with gastric variceal hemorrhage: Endoscopic N-Butyl-2Cyanoacrylate injection versus balloon-occluded retrograde transvenous obliteration. Hepatology 24:372-378, 2009 14. Yamagami T, Kato T, Hirota T, et al: Infusion of 50% glucose solution before injection of ethanolamine oleate during balloon-occluded retrograde transvenous obliteration. Radiology 51:334-338, 2007 15. Kitamoto M, Imamura M, Kamada K, et al: Balloon-occluded retrograde transvenous obliteration of gastric fundal varices with hemorrhage. AJR Am J Roentgenol 178:1167-1174, 2002 16. Choi YH, Yoon CJ, Park JH, et al: Balloon-occluded retrograde transvenous obliteration for gastric variceal bleeding: Its feasibility compared with transjugular intrahepatic portosystemic shunt. Korean J Radiol 4:109-116, 2003