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DOI: 10.1055/s-2008-1077400
© Georg Thieme Verlag KG Stuttgart · New York
EUS for portal hypertension: a comprehensive and critical appraisal of clinical and experimental indications
M. S. Bhutani, MD, FACG
Department of Gastroenterology, Hepatology and Nutrition, Unit 436
University of Texas
MD Anderson Cancer Center
Faculty Center
Room 10.2028
1515 Holcombe Blvd
Houston
TX 77030-4009
USA
Fax: +1-713-5634398
Email: Manoop.Bhutani@mdanderson.org
Publication History
submitted 31 December 2007
accepted after revision 14 April 14 2008
Publication Date:
07 July 2008 (online)
- Introduction
- Visualization of vascular and structural changes within and outside esophageal, gastric, and rectal walls in patients with portal hypertension
- EUS study of hemodynamic changes in portal hypertension
- Identification of risk factors for variceal bleeding, recurrence, and rebleeding after endoscopic therapy
- EUS assistance in and assessment of endoscopic therapy of bleeding esophageal, gastric, and duodenal varices
- Role of EUS in assessment of pharmacological effects of drugs used in the treatment of portal hypertension
- Conclusions
- Acknowledgments
- References
Endoscopic ultrasonography (EUS) has significantly improved our understanding of the complex vascular structural changes that occur in portal hypertension and their clinical and prognostic significance. EUS in combination with color Doppler technique enables us to study the hemodynamic changes in the portal venous system noninvasively, and to determine objectively the effect of different pharmacological agents on portal hypertension. EUS has also found some role in the treatment and follow up of esophageal and gastric varices. It may play a clinical role in the diagnosis of gastric, duodenal, and rectal varices. Recently reported EUS-based devices that measure variceal wall tension and intravariceal pressure noninvasively could have an impact on the identification of patients at high risk of variceal bleeding with the aim of initiating prophylactic treatment, and in the assessment of patients’ responses to drug therapy of portal hypertension. EUS is occasionally very helpful in the clinical management of portal hypertension. It is an interesting and important research tool for many experimental indications that are not routinely applied in clinical practice at this time.
#Introduction
Endoscopic ultrasonography (EUS) has become an important modality in the diagnosis and treatment of portal hypertension. McCormack and colleagues in 1983 described an endoscopic Doppler technique to study blood flow in esophageal varices in patients with portal hypertension [1]. Caletti et al. [2] in 1986 subsequently used conventional EUS to image esophagogastric varices in patients with portal hypertension. This review summarizes current literature regarding the role of EUS in the management of portal hypertension ([Tables 1] and [2]).
| Visualization of portal and azygos venous system changes |
| Assessment and diagnosis of gastric fundic varices |
| Diagnosis of watermelon stomach |
| Diagnosis and confirmation of ectopic duodenal varices |
| Demonstration of rectal venous system changes |
| Hemodynamic study of left gastric and azygos venous changes |
| Assessment and assistance with endoscopic therapy of esophageal and gastric varices |
| Assessment of pharmacological effects of drugs on portal venous pressure |
| Submucosal anechoic vascular structures in esophageal mucosa |
| Curved, serpiginous, and dilated submucosal anechoic vascular structures in gastric mucosa |
| Paraesophageal and paragastric collateral veins |
| Thickening of gastric mucosal and submucosal layers |
| Dilated azygos vein and increased blood flow |
| Dilated portal vein |
| Increased diameter of left gastric vein |
| Dilated thoracic duct |
Visualization of vascular and structural changes within and outside esophageal, gastric, and rectal walls in patients with portal hypertension
#Changes in the intrinsic and extrinsic venous plexuses
Accurate knowledge and a good understanding of vascular changes in the lower esophagus and upper stomach in patients with portal hypertension are essential for proper management of patients with variceal hemorrhage. The vascular anatomy of the intrinsic venous plexus at the lower esophagus is composed of four layers: intraepithelial channels, superficial venous plexus, deep venous plexus, and adventitial veins [3] [4]. All these venous channels are engorged in patients with portal hypertension. The dilated deep submucosal veins are seen as variceal columns at endoscopy, while the dilated adventitial veins form the paraesophageal collaterals, which are not visible by the conventional endoscopy. EUS provides high-resolution images of this region [5], with the esophageal and gastric wall appearing as a multilayered structure with histologic correlates [6] ([Fig. 1]).
Fig. 1 Schematic representation of esophageal variceal findings by EUS.
In patients with portal hypertension, both esophageal and gastric varices and periesophageal and perigastric collateral veins can be visualized adequately by endosonography [7]. Esophageal and gastric varices appear as submucosal anechoic vascular structures by EUS, as do dilated periesophageal and perigastric vessels.
#EUS and study of esophageal varices
In earlier EUS studies the sensitivity in detection of esophageal varices was 14 % in patients with grade 1 esophageal varices, 50 % in patients with grade 2, and 78 % in those with grade 3 varices, but it was superior to that of endoscopy in the detection of gastric varices [7]. Similar observations were made in another study suggesting that the higher the endoscopic grade of esophageal varices, the higher the sensitivity of EUS [8] ([Fig. 2]).
Fig. 2 a Endoscopic image of esophageal varices. b EUS image of esophageal varices: variceal lumens are visualized in the submucosal layer.
Subsequently, it was suggested that the success rate in visualizing small esophageal varices by EUS can be improved by using a small water-filled balloon during the procedure [9]. Small 20-Hz ultrasound transducers with high resolution and less compression artifact allow better visualization of esophageal varices by EUS, similar to upper endoscopy [10] [11]. In another study, videotaped high-resolution endoluminal sonography (HRES) was used to image and measure esophageal varices and compared with videotaped endoscopy in patients with portal hypertension [12]. The investigators found that HRES allows quantitative measurement of variceal size and is a more sensitive and reproducible imaging modality than endoscopy for the detection and size estimation of esophageal varices. Similarly, a high-frequency ultrasound miniature probe (UMP) inserted through the accessory channel of an endoscope allows better visualization of esophageal varices [13]. The hematocystic spots on the variceal surface appear as saccular-aneurysm-like projections representing focal weaknesses on the variceal wall, as seen with HRES, which explains why they are associated with an increased risk of variceal hemorrhage [14].
#EUS and study of gastric varices
Gastric varices as shown by EUS appear as submucosal curved, serpiginous, and dilated anechoic structures [7] ([Fig. 3]). Iwase et al. visualized small gastric varices that were difficult to detect by endoscopy by using color Doppler EUS (CD-EUS) [15], while recently Wong et al. were able to demonstrate the presence of a continuous venous hum with an endoscopic Doppler ultrasound probe [16]. Iwase et al. [15] also showed that the feeding vein for the junctional type of gastric varices was mainly the left gastric vein, whereas the fundic type of gastric varices were fed by the short gastric vein. These findings are similar to those of the angiographic studies [17]. A number of reported studies comparing EUS with conventional endoscopy in the detection of gastric varices confirm its superiority over endoscopy [7] [8] [9] [18] [19] [20].
Fig. 3 a Endoscopic image of gastric varices. b EUS image of gastric varices: variceal lumens are visualized in the submucosal layer.
EUS and study of esophageal and gastric variceal collaterals
Collateral veins are found adjacent to or outside the esophageal wall in all patients with esophageal varices but not in any control subjects [21]. Caletti et al. showed that paraesophageal veins were detected in 57 % of patients with grade 1 esophageal varices, in 89 % of patients with grade 2 varices, and in 100 % of patients with grade 3 varices [7]. They also found a direct correlation between the endoscopic grade of esophageal varices and the diameter of paraesophageal collateral veins at EUS. Another group of investigators classified their patients according to the number and size of their paraesophageal collateral veins. They compared the diameter of the paraesophageal collaterals with that of the splenic vein and considered the collaterals as large if they were wider than the splenic vein [22]. On the other hand, Leung et al. classified these collaterals into large if they were 5 mm or more in size and small if they were smaller than 5 mm [23] ([Fig. 4]).
Using a UMP, the esophageal collateral veins can be divided into two groups according to their location with respect to the outermost wall (muscularis externa) of the esophagus: periesophageal collateral veins and paraesophageal collateral veins [21]. Periesophageal collateral veins appear as small vessels adjacent to the muscularis externa of the esophagus, whereas paraesophageal collateral veins appear as large vessels separated from the muscularis externa of the esophagus by a clear hyperechoic border.
Paraesophageal and paragastric varices as detected by EUS correlate with the presence and severity of liver disease and portal hypertension and may be risk factors for variceal hemorrhage [24].
Fig. 4 EUS image of esophageal varices: paraesophageal collateral veins are visualized outside the esophageal wall (arrows).
EUS and study of esophageal and gastric perforators
As early as 1983, McCormack et al. using a Doppler ultrasound probe recorded that blood flow in the submucosal esophageal varices is bidirectional at different levels in the same varix [25]. This was explained by the presence and demonstration of functioning perforating veins joining esophageal varices to periesophageal veins, particularly at the lower end of the esophagus. Perforating veins were also detected and described by transesophageal real-time two-dimensional Doppler ultrasonography by Sukigara et al. [26].
A subsequent study has further defined esophageal perforating veins as veins connecting esophageal varices with perivariceal or paravariceal collateral veins [21]. CD-EUS was used in another study to assess the presence and diameter of the perforating veins in the region of the palisade and perforating zones [27].
#EUS and study of gastric mucosal changes
EUS can detect portal hypertensive gastropathy [28]. The gastric mucosa commonly has an altered appearance at endoscopic examination in patients with cirrhosis. The thickness of the gastric mucosal and submucosal layers doubles, most likely because of the relative outflow obstruction of venous and lymphatic flow. Whether this EUS finding is related to the endoscopic findings of portal hypertensive gastropathy, however, could not be determined because of the high prevalence of endoscopic mucosal abnormalities in cirrhotic patients [24].
Chen et al. used EUS in the differential diagnosis of giant gastric folds [29]. They found that all patients with gastric varices had anechoic tortuous varicose veins in the submucosal layer. However, EUS images of gastric wall lymphangiectasis were similar to those of gastric varices. In a small case series, EUS was used to diagnose watermelon stomach in patients with portal hypertension. EUS allowed precise documentation and localization of ectatic intramural vessels in the mucosa and submucosa, which appeared as distinct echo-poor vascular structures in the submucosa and the mucosa [30].
#EUS and study of azygos vein dilation
Caletti et al. and other groups have reported azygos vein dilation in patients with cirrhosis and portal hypertension [7] [24] [31]. Such dilation of the azygos vein may be due to the shunting of a major portion of blood from the portal circulation to the systemic circulation via esophageal collateral blood vessels which drain into the superior vena cava through the azygos venous system. Azygos vein diameter has been found to be significantly correlated with Child’s class among patients without prior variceal hemorrhage [24].
However, in another study patients with advanced liver disease as reflected by Child–Pugh grading did not have significantly larger azygos vein diameters [32]. Other reported causes of azygos vein dilation are: congestive heart failure, inferior vena cava thrombosis, right atrial mural thrombosis, pulmonary embolism, congenital azygos continuation to the inferior vena cava, and arteriovenous fistula [33].
#EUS and study of the left gastric vein
The morphology and hemodynamics of the left gastric vein (LGV) in patients with portal hypertension was studied to evaluate factors affecting the development of esophageal varices [27]. It was shown that the diameter of the LGV trunk increases with increasing variceal size. This study also demonstrated the branching pattern of the LGV and its relationship to collateral channels. This branching pattern was found to be closely associated with the development of esophageal varices, since dominance of the anterior branch may be responsible for directing LGV blood flow toward varices at the level of the proximal stomach [27].
Preliminary studies [27] [34] suggested that either a high hepatofugal flow velocity in the LGV or an anterior branch dominant pattern seen under CD-EUS was a possible contributing factor for variceal recurrence after endoscopic treatment. The same group recently published a larger study of 68 patients [35] treated for moderate or large esophageal varices with variceal ligation and sclerotherapy after CD-EUS. The authors concluded that their results suggest that patients showing anterior branch dominance and rapid hepatofugal flow velocity in the LGV on CD-EUS examination may be at high risk of early recurrence of esophageal varices.
#EUS and study of thoracic duct changes
Thoracic duct morphological changes detected by EUS in patients with portal hypertension were initially reported by Parasher and co-workers [36]. It was suggested that a dilated thoracic duct found at EUS may be a sign of advanced cirrhosis with ascites and esophageal varices. Thoracic duct dilation in patients with cirrhosis was also reported later in another study [24].
#EUS and study of rectal mucosa and rectal venous system changes
Colorectal varices and congestive rectopathy or colopathy have been reported in patients with portal hypertension [37]. EUS shows rectal varices as round, oval, or longitudinal echo-free structures that run a long course in the submucosa, whereas perirectal veins appear as round, oval, or longitudinal echo-free structures outside the rectal wall. Rectal EUS was found to be superior to endoscopy in detecting rectal varices irrespective of size, whereas endoscopy could detect only larger varices. Additionally, rectal EUS could detect perforating veins connecting submucosal to perirectal veins in 28.3 % of patients with portal hypertension. In congestive rectopathy due to portal hypertension, rectal EUS showed multiple small dilated vessels (small round echo-free structures) in the submucosa.
Rectal EUS may play a role in confirming endoscopically identified or suspected rectal varices and may help differentiate portal rectopathy from inflammatory colitis [38].
#EUS study of hemodynamic changes in portal hypertension
#EUS study of portal venous system
Among other EUS findings suggestive of portal hypertension are portal vein enlargement and the presence of collateral veins. The feasibility of direct EUS-guided portal vein catheterization using a 22-gauge needle and accurate pressure measurement has been demonstrated in animal models [39]. Patency of the portal or splenic vein is defined by a continuous, low-velocity pulsed and color Doppler signal within the vessel. On the other hand, venous thrombosis is demonstrated by the absence of flow within the vessel, with or without the finding of stationary echoes (solid thrombosis) within the lumen [40] [41]. Furthermore, duplex Doppler and CD-EUS can be used to evaluate a splenorenal shunt. Shunt stenosis can be evaluated by measuring the peak systolic velocity at different points along the course of the shunt. Any evidence of an increase in peak velocity along the shunt associated with a greater than 70 % luminal narrowing and presence of adjacent collaterals is considered a sign of significant stenosis of the shunt [42].
#EUS study of hemodynamic changes in azygos venous system
Azygos blood flow has been found to be four to six times higher than normal in patients with cirrhosis and portal hypertension. Thus, measurement of azygos blood flow is an index of blood flow through gastroesophageal collateral blood vessels and esophageal varices [43]. CD-EUS has been used to study the azygos vein in the assessment of patients with cirrhosis and portal hypertension [32]. There are limited reports on the validity of using CD-EUS for azygos blood flow measurements against the standard thermodilution technique in patients with cirrhosis and portal hypertension [44] [45]. Hemodynamic changes in the azygos vein which occur after variceal obliteration by endoscopic injection sclerotherapy in patients with portal hypertension and bleeding esophageal varices has also been studied [46]. There appears to be significant increase in azygos vein diameter and blood flow volume index without significant changes in maximal velocity following variceal obliteration.
#EUS study of hemodynamic changes in left gastric vein
As previously described, the hemodynamics and morphology of the LGV have been investigated in patients with portal hypertension using CD-EUS [27]. Hepatofugal flow velocity was found to increase with increasing size of the varices and was significantly different between patients with small varices (F1) and patients with medium varices (F2), and between patients with F2 and F3 (large) varices. The direction of blood flow in the perforating veins was toward the esophageal varices in all patients.
#EUS measurement of esophageal variceal tension
Jackson et al. used HRES to measure variceal wall thickness and radius, and performed direct needle puncture to measure the intravariceal pressure in patients with portal hypertension [47]. To avoid risk of variceal bleeding from needle puncture, Miller et al. have reported success in developing a noninvasive EUS-based device to measure intravariceal pressure in a varix model by placing a 20-MHz ultrasound transducer in a latex balloon catheter sheath and attaching the catheter to a pressure transducer [48] [49]. This assembly was then placed in a notched overtube of special design and placed through a biopsy channel of a therapeutic endoscope and tested on variceal models made of nitrocellulose dialysis tubes of various lengths and filled with water. This device demonstrated a low percent error (< 10 %) and a high correlation to the actual intravariceal pressure (r = 0.96). However, larger clinical trials of this device in human subjects are needed before its clinical use.
#Identification of risk factors for variceal bleeding, recurrence, and rebleeding after endoscopic therapy
#EUS identification of risk factors for variceal recurrence and rebleeding after endoscopic therapy
The role of paraesophageal collateral veins and perforating veins on the outcome of endoscopic injection sclerotherapy (EIS) for esophageal varices has been studied using EUS [50]. The number and size of paraesophageal collaterals were found to be significantly less in the group of patients who responded to EIS than in the nonresponder group. Perforating veins were visualized more frequently in the nonresponders. These data suggest that successful eradication of esophageal varices by EIS is associated with the disappearance of perforating veins in the lower esophagus and a reduction in the number and size of paraesophageal collaterals. Similar results were reported by Irisawa et al. [51].
In a pilot study on modified variceal ligation using CD-EUS, the nonrecurrence group of patients tended to show undeveloped (grade 1) gastric varices and/or developed (grade III) periesophageal collateral veins [52].
The prevalence of paraesophageal and gastric varices in patients following endoscopic therapy (band ligation versus injection sclerotherapy) for bleeding esophageal varices has been compared using EUS [19]. This study found that the prevalence of paraesophageal varices was significantly higher in the ligation group than in the sclerotherapy group. Additionally, patients with esophageal varices treated with endoscopic variceal ligation and evidence of severe as opposed to mild-grade perforating veins before treatment tended to have a higher recurrence rate [18].
#EUS assistance in and assessment of endoscopic therapy of bleeding esophageal, gastric, and duodenal varices
#EUS assistance in and assessment of esophageal variceal ligation
Endoscopic variceal ligation (EVL) is a simple, safe, and effective technique for treating esophageal varices [53]. However, EVL is associated with more frequent short-term variceal recurrence than is EIS.
Nagamine et al., in order to decrease variceal recurrence, conducted a pilot study of a “modified” EVL technique in conjunction with a UMP. Esophageal varices were imaged by UMP followed by intensive EVL therapy [52]. EVL was repeated every 2nd week until varices showed complete eradication or marked reduction and the red color sign became negative. The reported intermediate-term (12 – 24 months) outcome of patients treated by this technique was good.
#EUS assistance in and assessment of endoscopic injection sclerotherapy
Directed delivery of sclerosant under EUS guidance may decrease the number of sessions required for obliteration of esophageal varices and may also decrease the recurrence rate of esophageal varices after initial obliteration [54].
EIS for the eradication of esophageal varices was recently compared with EUS-guided EIS in a randomized controlled trial that concluded that EUS-guided EIS is not only as safe and effective as EIS alone in the eradication of esophageal varices, but also that recurrence tends to be less frequent and more delayed [55].
EUS in combination with percutaneous transhepatic portography has also been found to be useful in the preoperative evaluation in selecting devascularization surgery for esophagogastric varices, although surgical outcome remained unchanged [56].
#EUS assistance in and assessment of endoscopic therapy of gastric varices
Management of bleeding gastric varices can be a challenge. EUS-guided cyanoacrylate glue injection of gastric varices has been attempted with success [15] [57]. There is also a recently reported case series of EUS-guided cyanoacrylate injection into the perforating feeding veins in gastric varices for eradication [58].
Also recently, preoperative EUS was used to determine the mode of devascularization surgery in patients with isolated gastric varices [59].
#EUS and management of duodenal varices
Duodenal varices can result in fatal massive bleeding [60]. EUS is a useful tool to confirm diagnosis of suspected duodenal varices [60] [61]. Endosonographically, duodenal varices usually appear as echo-free dilated venous spaces in the submucosal or serosal layer [61] [62]. Yeh et al. used EUS to confirm the nature of a suspected bleeding duodenal varix before its successful band ligation in a patient with liver cirrhosis and unresectable hepatocellular carcinoma [63].
#Role of EUS in assessment of pharmacological effects of drugs used in the treatment of portal hypertension
#Clinical role of EUS in assessment of drug effects on azygos blood flow
It has been demonstrated that azygos blood flow (AzBF) is an index of blood flow through gastroesophageal collateral vessels in patients with portal hypertension, which was found to be four to six times higher than normal in patients with cirrhosis and portal hypertension [43]. It also correlates with the severity of portal hypertension [64]. Lee et al. studied the effects of a bolus injection of 2 mg terlipressin, 250 µg somatostatin, or saline solution (control) on AzBF in patients with portal hypertension, by using linear-array CD-EUS [32]. They found that after bolus injection of terlipressin and somatostatin, there was a marked decrease in AzBF (24 % and 37 % respectively at 1 minute, 42 % and 19 % at 5 minutes, and 40 % for both at 10 minutes) compared with baseline. The action of somatostatin appeared to be more dramatic in the first minute after bolus injection. Moreover, somatostatin, unlike terlipressin, did not cause a significant reduction in pulse rate or arterial blood pressure. This study illustrates the well-known selective vasoconstrictive effects of somatostatin on the splanchnic circulation.
A similar effect of drugs on AzBF was demonstrated in other studies [44] [45].
#Potential role of EUS in assessment of effects of drugs on portal hypertension
A high-resolution EUS-based method can be used to determine variceal volume in a varix model and in patients with portal hypertension and esophageal varices [65]. Since these measurements correspond closely with the actual measurements, this technique can possibly be used in the assessment of the effects of pharmacological therapy on portal hypertension.
#Conclusions
In conclusion, in occasional patients EUS is really helpful in managing portal hypertension, particularly in diagnosing varices at locations such as the proximal stomach, the duodenum, or the rectum. However, on the basis of this detailed and critical review, other indications for EUS in portal hypertension are very limited or at an experimental stage. EUS does not currently have a routine role in monitoring pharmacological therapy for portal hypertension, and considering its invasiveness and the expertise required to use it, this seems unlikely to change in the near future. The same is true for monitoring the results of endoscopic therapy of esophageal varices. Further work is needed on the clinical relevance of periesophageal veins versus paraesophageal veins. Also, from a clinical point of view, assessing the diameter of the thoracic duct and confirming the presence of red spots on varices or of watermelon stomach is not clinically relevant at this time despite the fact that EUS has been helpful in furthering our understanding of many physiologic and structural alterations in portal hypertension. Routine measurement of esophageal variceal pressure using EUS has not been clinically established or standardized. In conclusion, therefore, EUS is occasionally very helpful in the management of portal hypertension, and it is an interesting and important research tool, but in the large majority of cases a significant role for EUS has not (yet) been defined, with many areas of potential research by investigators with interest in this application of EUS.
#Acknowledgments
Dr. M. El-Saadany and Dr S. Jalil contributed equally to the manuscript. Dr. M. El-Saadany was the recipient of the American College of Gastroenterology International training grant in 2002.
Competing interests: None
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- 44 Hansen E F, Bendtsen F, Brinch K, Moller S. et al . Endoscopic Doppler ultrasound for measurement of azygos blood flow. Validation against thermodilution and assessment of pharmacological effects of terlipressin in portal hypertension. Scand J Gastroenterol. 2001; 36 318-325
- 45 Nishida H, Giostra E, Spahr L. et al . Validation of color Doppler EUS for azygos blood flow measurement in patients with cirrhosis: application to the acute hemodynamic effects of somatostatin, octreotide, or placebo. Gastrointest Endosc. 2001; 54 24-30
- 46 Kassem A M, Salama Z A, Zakaria M S. et al . Endoscopic ultrasonographic study of the azygos vein before and after endoscopic obliteration of esophagogastric varices by injection sclerotherapy. Endoscopy. 2000; 32 630-634
- 47 Jackson F W, Adrain A L, Black M, Miller L S. Calculation of esophageal variceal wall tension by direct sonographic and manometric measurements. Gastrointest Endosc. 1999; 50 247-251
- 48 Miller E S, Kim J K, Gandehok J. et al . A new device for measuring esophageal variceal pressure. Gastrointest Endosc. 2002; 56 284-291
- 49 Miller L S, Dai Q, Thomas A. et al . A new ultrasound-guided esophageal variceal pressure-measuring device. Am J Gastroenterol. 2004; 99 1267-1273
- 50 Dhiman R K, Choudhuri G, Saraswat V A. et al . Role of paraoesophageal collaterals and perforating veins on outcome of endoscopic sclerotherapy for oesophageal varices: an endosonographic study. Gut. 1996; 38 759-764
- 51 Irisawa A, Saito A, Obara K. et al . Endoscopic recurrence of esophageal varices is associated with the specific EUS abnormalities: severe periesophageal collateral veins and large perforating veins. Gastrointest Endosc. 2001; 53 77-84
- 52 Nagamine N, Ueno N, Tomiyama T. et al . A pilot study on modified endoscopic variceal ligation using endoscopic ultrasonography with color Doppler function. Am J Gastroenterol. 1998; 93 150-155
- 53 Van Stiegmann G, Goff J S. Endoscopic esophageal varix ligation: preliminary clinical experience. Gastrointest Endosc. 1988; 34 113-117
- 54 Lahoti S, Catalano M F, Alcocer E. et al . Obliteration of esophageal varices using EUS-guided sclerotherapy with color Doppler. Gastrointest Endosc. 2000; 51 331-333
- 55 de Paulo G A, Ardengh J C, Nakao F S, Ferrari A P. Treatment of esophageal varices: a randomized controlled trial comparing endoscopic sclerotherapy and EUS-guided sclerotherapy of esophageal collateral veins. Gastrointest Endosc. 2006; 63 396-402; quiz 463
- 56 Hsieh J S, Jan C M, Lu C Y. et al . Preoperative evaluation of endoscopic ultrasonography and portography in selecting devascularization surgery for esophagogastric varices. Am Surg. 2005; 71 439-444
- 57 Lee Y T, Chan F K, Ng E K. et al . EUS-guided injection of cyanoacrylate for bleeding gastric varices. Gastrointest Endosc. 2000; 52 168-174
- 58 Romero-Castro R, Pellicer-Bautista F J, Jimenez-Saenz M. et al . EUS-guided injection of cyanoacrylate in perforating feeding veins in gastric varices: results in 5 cases. Gastrointest Endosc. 2007; 66 402-407
- 59 Hsieh J S, Wang W M, Perng D S. et al . Modified devascularization surgery for isolated gastric varices assessed by endoscopic ultrasonography. Surg Endosc. 2004; 18 666-671
- 60 Wu C S, Chen C M, Chang K Y. Endoscopic injection sclerotherapy of bleeding duodenal varices. J Gastroenterol Hepatol. 1995; 10 481-483
- 61 Sung J Y, Chung S C, Leung H T. et al . Duodenal varices in hepatocellular carcinoma. Endoscopy. 1993; 25 194-196
- 62 Nardone G, Budillon G. Treatment of duodenal varices by endoscopic sclerotherapy. Gastrointest Endosc. 1991; 37 407-408
- 63 Yeh Y Y, Hou M C, Lin H C. et al . Case report: successful obliteration of a bleeding duodenal varix using endoscopic ligation. J Gastroenterol Hepatol. 1998; 13 591-593
- 64 Braillon A, Cales P, Valla D. et al . Influence of the degree of liver failure on systemic and splanchnic haemodynamics and on response to propranolol in patients with cirrhosis. Gut. 1986; 27 1204-1209
- 65 Chung C Y, McCray W H, Dhaliwal S. et al . Three-dimensional esophageal varix model quantification of variceal volume by high-resolution endoluminal US. Gastrointest Endosc. 2000; 52 87-90
M. S. Bhutani, MD, FACG
Department of Gastroenterology, Hepatology and Nutrition, Unit 436
University of Texas
MD Anderson Cancer Center
Faculty Center
Room 10.2028
1515 Holcombe Blvd
Houston
TX 77030-4009
USA
Fax: +1-713-5634398
Email: Manoop.Bhutani@mdanderson.org
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- 43 Bosch J, Mastai R, Kravetz D. et al . Measurement of azygos venous blood flow in the evaluation of portal hypertension in patients with cirrhosis. Clinical and haemodynamic correlations in 100 patients. J Hepatol. 1985; 1 125-139
- 44 Hansen E F, Bendtsen F, Brinch K, Moller S. et al . Endoscopic Doppler ultrasound for measurement of azygos blood flow. Validation against thermodilution and assessment of pharmacological effects of terlipressin in portal hypertension. Scand J Gastroenterol. 2001; 36 318-325
- 45 Nishida H, Giostra E, Spahr L. et al . Validation of color Doppler EUS for azygos blood flow measurement in patients with cirrhosis: application to the acute hemodynamic effects of somatostatin, octreotide, or placebo. Gastrointest Endosc. 2001; 54 24-30
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- 47 Jackson F W, Adrain A L, Black M, Miller L S. Calculation of esophageal variceal wall tension by direct sonographic and manometric measurements. Gastrointest Endosc. 1999; 50 247-251
- 48 Miller E S, Kim J K, Gandehok J. et al . A new device for measuring esophageal variceal pressure. Gastrointest Endosc. 2002; 56 284-291
- 49 Miller L S, Dai Q, Thomas A. et al . A new ultrasound-guided esophageal variceal pressure-measuring device. Am J Gastroenterol. 2004; 99 1267-1273
- 50 Dhiman R K, Choudhuri G, Saraswat V A. et al . Role of paraoesophageal collaterals and perforating veins on outcome of endoscopic sclerotherapy for oesophageal varices: an endosonographic study. Gut. 1996; 38 759-764
- 51 Irisawa A, Saito A, Obara K. et al . Endoscopic recurrence of esophageal varices is associated with the specific EUS abnormalities: severe periesophageal collateral veins and large perforating veins. Gastrointest Endosc. 2001; 53 77-84
- 52 Nagamine N, Ueno N, Tomiyama T. et al . A pilot study on modified endoscopic variceal ligation using endoscopic ultrasonography with color Doppler function. Am J Gastroenterol. 1998; 93 150-155
- 53 Van Stiegmann G, Goff J S. Endoscopic esophageal varix ligation: preliminary clinical experience. Gastrointest Endosc. 1988; 34 113-117
- 54 Lahoti S, Catalano M F, Alcocer E. et al . Obliteration of esophageal varices using EUS-guided sclerotherapy with color Doppler. Gastrointest Endosc. 2000; 51 331-333
- 55 de Paulo G A, Ardengh J C, Nakao F S, Ferrari A P. Treatment of esophageal varices: a randomized controlled trial comparing endoscopic sclerotherapy and EUS-guided sclerotherapy of esophageal collateral veins. Gastrointest Endosc. 2006; 63 396-402; quiz 463
- 56 Hsieh J S, Jan C M, Lu C Y. et al . Preoperative evaluation of endoscopic ultrasonography and portography in selecting devascularization surgery for esophagogastric varices. Am Surg. 2005; 71 439-444
- 57 Lee Y T, Chan F K, Ng E K. et al . EUS-guided injection of cyanoacrylate for bleeding gastric varices. Gastrointest Endosc. 2000; 52 168-174
- 58 Romero-Castro R, Pellicer-Bautista F J, Jimenez-Saenz M. et al . EUS-guided injection of cyanoacrylate in perforating feeding veins in gastric varices: results in 5 cases. Gastrointest Endosc. 2007; 66 402-407
- 59 Hsieh J S, Wang W M, Perng D S. et al . Modified devascularization surgery for isolated gastric varices assessed by endoscopic ultrasonography. Surg Endosc. 2004; 18 666-671
- 60 Wu C S, Chen C M, Chang K Y. Endoscopic injection sclerotherapy of bleeding duodenal varices. J Gastroenterol Hepatol. 1995; 10 481-483
- 61 Sung J Y, Chung S C, Leung H T. et al . Duodenal varices in hepatocellular carcinoma. Endoscopy. 1993; 25 194-196
- 62 Nardone G, Budillon G. Treatment of duodenal varices by endoscopic sclerotherapy. Gastrointest Endosc. 1991; 37 407-408
- 63 Yeh Y Y, Hou M C, Lin H C. et al . Case report: successful obliteration of a bleeding duodenal varix using endoscopic ligation. J Gastroenterol Hepatol. 1998; 13 591-593
- 64 Braillon A, Cales P, Valla D. et al . Influence of the degree of liver failure on systemic and splanchnic haemodynamics and on response to propranolol in patients with cirrhosis. Gut. 1986; 27 1204-1209
- 65 Chung C Y, McCray W H, Dhaliwal S. et al . Three-dimensional esophageal varix model quantification of variceal volume by high-resolution endoluminal US. Gastrointest Endosc. 2000; 52 87-90
M. S. Bhutani, MD, FACG
Department of Gastroenterology, Hepatology and Nutrition, Unit 436
University of Texas
MD Anderson Cancer Center
Faculty Center
Room 10.2028
1515 Holcombe Blvd
Houston
TX 77030-4009
USA
Fax: +1-713-5634398
Email: Manoop.Bhutani@mdanderson.org
Fig. 1 Schematic representation of esophageal variceal findings by EUS.
Fig. 2 a Endoscopic image of esophageal varices. b EUS image of esophageal varices: variceal lumens are visualized in the submucosal layer.
Fig. 3 a Endoscopic image of gastric varices. b EUS image of gastric varices: variceal lumens are visualized in the submucosal layer.
Fig. 4 EUS image of esophageal varices: paraesophageal collateral veins are visualized outside the esophageal wall (arrows).