EUS for portal hypertension: a comprehensive and critical appraisal of clinical and experimental indications

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.

• 1 McCormack T, Martin T, Smallwood R H. et al . Doppler ultrasound probe for assessment of blood-flow in oesophageal varices.  Lancet. 1983;  1 677-678
• 2 Caletti G C, Bolondi L, Zani L. et al . Detection of portal hypertension and esophageal varices by means of endoscopic ultrasonography.  Scand J Gastroenterol Suppl. 1986;  123 74-77
• 3 Hashizume M, Kitano S, Sugimachi K, Sueishi K. Three-dimensional view of the vascular structure of the lower esophagus in clinical portal hypertension.  Hepatology. 1988;  8 1482-1487
• 4 Kitano S, Terblanche J, Kahn D, Bornman P C. Venous anatomy of the lower oesophagus in portal hypertension: practical implications.  Br J Surg. 1986;  73 525-531
• 5 Rösch T. Endoscopic ultrasonography.  Endoscopy. 1992;  24 144-153
• 6 Kimmey M B, Martin R W, Haggitt R C. et al . Histologic correlates of gastrointestinal ultrasound images.  Gastroenterology. 1989;  96 433-441
• 7 Caletti G, Brocchi E, Baraldini M. et al . Assessment of portal hypertension by endoscopic ultrasonography.  Gastrointest Endosc. 1990;  36 S21-S27
• 8 Burtin P, Cales P, Oberti F. et al . Endoscopic ultrasonographic signs of portal hypertension in cirrhosis.  Gastrointest Endosc. 1996;  44 257-261
• 9 Choudhuri G, Dhiman R K, Agarwal D K. Endosonographic evaluation of the venous anatomy around the gastro-esophageal junction in patients with portal hypertension.  Hepatogastroenterology. 1996;  43 1250-1255
• 10 Liu J B, Miller L S, Feld R I. et al . Gastric and esophageal varices: 20-MHz transnasal endoluminal US.  Radiology. 1993;  187 363-366
• 11 Nishizono M, Haraguchi Y, Eto T. et al . Endoscopic ultrasonography using a 15/20 MHz probe in a direct contact technique: evaluation and application in esophageal and gastric varices.  Fukuoka Igaku Zasshi. 1994;  85 251-255
• 12 Miller L S, Schiano T D, Adrain A. et al . Comparison of high-resolution endoluminal sonography to video endoscopy in the detection and evaluation of esophageal varices.  Hepatology. 1996;  24 552-555
• 13 Suzuki T, Matsutani S, Umebara K. et al . EUS changes predictive for recurrence of esophageal varices in patients treated by combined endoscopic ligation and sclerotherapy.  Gastrointest Endosc. 2000;  52 611-617
• 14 Schiano T D, Adrain A L, Vega K J. et al . High-resolution endoluminal sonography assessment of the hematocystic spots of esophageal varices.  Gastrointest Endosc. 1999;  49 424-427
• 15 Iwase H, Suga S, Morise K. et al . Color Doppler endoscopic ultrasonography for the evaluation of gastric varices and endoscopic obliteration with cyanoacrylate glue.  Gastrointest Endosc. 1995;  41 150-154
• 16 Wong R C, Farooq F T, Chak A. Endoscopic Doppler US probe for the diagnosis of gastric varices (with videos).  Gastrointest Endosc. 2007;  65 491-496
• 17 Watanabe K, Kimura K, Matsutani S. et al . 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
• 18 Konishi Y, Nakamura T, Kida H. et al . Catheter US probe EUS evaluation of gastric cardia and perigastric vascular structures to predict esophageal variceal recurrence.  Gastrointest Endosc. 2002;  55 197-203
• 19 Lo G H, Lai K H, Cheng J S. et al . Prevalence of paraesophageal varices and gastric varices in patients achieving variceal obliteration by banding ligation and by injection sclerotherapy.  Gastrointest Endosc. 1999;  49 428-436
• 20 Pontes J M, Leitao M C, Portela F A. et al . Endoscopic ultrasonography in the treatment of oesophageal varices by endoscopic sclerotherapy and band ligation: do we need it?.  Eur J Gastroenterol Hepatol. 1995;  7 41-46
• 21 Irisawa A, Obara K, Sato Y. et al . EUS analysis of collateral veins inside and outside the esophageal wall in portal hypertension.  Gastrointest Endosc. 1999;  50 374-380
• 22 Nakamura H, Endo M, Shimojuu K. et al . Esophageal varices evaluated by endoscopic ultrasonography: observation of collateral circulation during non-shunting operations.  Surg Endosc. 1990;  4 69-74; discussion 75
• 23 Leung V K, Sung J J, Ahuja A T. et al . Large paraesophageal varices on endosonography predict recurrence of esophageal varices and rebleeding.  Gastroenterology. 1997;  112 1811-1816
• 24 Faigel D O, Rosen H R, Sasaki A. et al . EUS in cirrhotic patients with and without prior variceal hemorrhage in comparison with noncirrhotic control subjects.  Gastrointest Endosc. 2000;  52 455-462
• 25 McCormack T T, Rose J D, Smith P M. et al . Perforating veins and blood flow in oesophageal varices.  Lancet. 1983;  2 1442-1444
• 26 Sukigara M, Komazaki T, Yamazaki T. et al . Colour flow mapping of oesophagogastric varices and vessels in and around the liver with trans-oesophageal real-time two-dimensional Doppler ultrasound.  Clin Radiol. 1987;  38 487-494
• 27 Hino S, Kakutani H, Ikeda K. et al . Hemodynamic assessment of the left gastric vein in patients with esophageal varices with color Doppler EUS: factors affecting development of esophageal varices.  Gastrointest Endosc. 2002;  55 512-517
• 28 Caletti G C, Brocchi E, Ferrari A. et al . Value of endoscopic ultrasonography in the management of portal hypertension.  Endoscopy. 1992;  24 Suppl 1 342-346
• 29 Chen T K, Wu C H, Lee C L. et al . Endoscopic ultrasonography in the differential diagnosis of giant gastric folds.  J Formos Med Assoc. 1999;  98 261-264
• 30 Avunduk C, Hampf F. Endoscopic ultrasound in the diagnosis of watermelon stomach.  J Clin Gastroenterol. 1996;  22 104-106
• 31 Salama Z A, Kassem A M, Giovannini M, Hunter M S. Endoscopic ultrasonographic study of the azygos vein in patients with varices.  Endoscopy. 1997;  29 748-750
• 32 Lee Y T, Sung J J, Yung M Y, Yu A L. et al . Use of color Doppler EUS in assessing azygos blood flow for patients with portal hypertension.  Gastrointest Endosc. 1999;  50 47-52
• 33 Shin M S. Clinical significance of azygos vein enlargement: radiographic recognition and etiologic analysis.  Clin Imaging. 1999;  23 236-240
• 34 Hino S, Kakutani H, Ikeda K. et al . Hemodynamic analysis of esophageal varices using color Doppler endoscopic ultrasonography to predict recurrence after endoscopic treatment.  Endoscopy. 2001;  33 869-72
• 35 Kuramochi A, Imazu H, Kakutani H. et al . Color Doppler endoscopic ultrasonography in identifying groups at a high-risk of recurrence of esophageal varices after endoscopic treatment.  J Gastroenterol. 2007;  42 219-224
• 36 Parasher V K, Meroni E, Malesci A. et al . Observation of thoracic duct morphology in portal hypertension by endoscopic ultrasound.  Gastrointest Endosc. 1998;  48 588-592
• 37 Goenka M K, Kochhar R, Nagi B, Mehta S K. Rectosigmoid varices and other mucosal changes in patients with portal hypertension.  Am J Gastroenterol. 1991;  86 1185-1189
• 38 Dhiman R K, Saraswat V A, Choudhuri G. et al . Endosonographic, endoscopic, and histologic evaluation of alterations in the rectal venous system in patients with portal hypertension.  Gastrointest Endosc. 1999;  49 218-227
• 39 Lai L, Poneros J, Santilli J, Brugge W. EUS-guided portal vein catheterization and pressure measurement in an animal model: a pilot study of feasibility.  Gastrointest Endosc. 2004;  59 280-283
• 40 Johansen K, Paun M. Duplex ultrasonography of the portal vein.  Surg Clin North Am. 1990;  70 181-190
• 41 Perisic-Savic M, Colovic R, Milosavljevic T, Ivanovic L. Splenic vein thrombosis. Diagnosed with Doppler ultrasonography.  Hepatogastroenterology. 1991;  38 557-560
• 42 Wiersema M J, Chak A, Kopecky K K, Wiersema L M. Duplex Doppler endosonography in the diagnosis of splenic vein, portal vein, and portosystemic shunt thrombosis.  Gastrointest Endosc. 1995;  42 19-26
• 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
• 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