Accepted Article
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Review
Potential application of interventional endoscopic ultrasonography for the treatment of esophageal and gastric varices1
Takuto Hikichi1, Katsutoshi Obara1, Shin-ichi Nakamura2, Atsushi Irisawa3, and Hiromasa Ohira4
1
Department of Endoscopy, Fukushima Medical University Hospital, Fukushima, Japan,
2
Department of Gastroenterology, Tokyo Women’s Medical University Hospital, Tokyo,
Japan, 3Department of Gastroenterology, Fukushima Medical University Aizu Medical
Center, Aizuwakamatsu, Japan, 4Department of Gastroenterology and Rheumatology, Fukushima Medical University School of Medicine, Fukushima, Japan.
Running title: Interventional EUS for GI varices
Correspondence: Takuto Hikichi, MD, PhD,
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/den.12436
1
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Associate Professor, Department of Endoscopy, Fukushima Medical University Hospital, 1 Hikarigaoka, Fukushima city, Fukushima, 960-1295, Japan Tel: +81-24-547-1583, Fax: +81-24-547-1586, Email: [email protected]
2
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Abstract
Interventional endoscopic ultrasonography (EUS) has been developed mainly for the treatment of pancreatico-biliary disorders (e.g., cyst drainage for pancreatic pseudocysts, biliary drainage for malignant biliary obstruction, and celiac plexus neurolysis). Recently, the application of interventional EUS has been expanded to a new field, the treatment of gastrointestinal varices. There have been several studies examining this new technique for the treatment of esophageal and gastric varices. In this review, we have aimed to summarize the current status of interventional EUS for the treatment of esophageal and gastric varices (e.g., EUS-guided coil deployment for gastric varices) and to clarify the clinical feasibility of this procedure.
Key words: coil, cyanoacrylate, endoscopic ultrasonography (EUS), interventional EUS, varix
3
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INTRODUCTION Bleeding from esophageal and gastric varices often causes catastrophic
hemodynamic deterioration and is one of the most common causes of death among patients with portal hypertension such as those suffering from liver cirrhosis. Therefore, the successful treatment of bleeding esophageal and gastric varices can significantly improve the outcome for such patients.1-9 Varices that are large and/or red color sign are considered to be at high risk of bleeding and are treated prophylactically by endoscopic1-3 or interventional radiology (IVR)4 therapy. There are two types of endoscopic treatment for esophageal varices, namely endoscopic injection sclerothrapy (EIS) using sclerosants5 and endoscopic variceal ligation (EVL).6 Regarding gastric varices with large variceal lumen and rapid blood flow, cyanoacylate glue (CA) injection1,9 under conventional endoscopy has been the first choice treatment especially in cases of bleeding. However, conventional endoscopic approach is “blind.” Because we cannot see directly the depth of the varix, we sometimes cannot inject CA or sclerosants into the varices. IVR therapy such as balloon-occluded retrograde transvenous obliteration (B-RTO)4 has been performed for prophylactic gastric varices cases. However, a large volume of sclerosant is required and the catheter must remain in position for several hours in order to perform B-RTO. Interventional endoscopic ultrasonography (EUS), including EUS-guided fine
needle aspiration, was developed by Vilmann et al.10 in 1992 and has been popular in the 4
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diagnosis of pancreatic tumors,11,12 gastrointestinal (GI) subepithelial tumors, pancreatic
pseudocyst drainage,13 celiac plexus neurolysis, and other procedures. Recently, several studies utilized the interventional EUS technique in the treatment of GI varices. The biggest advantage of interventional EUS is that it allows the surgeon to see the varix lumen directly in the real-time. Here, we summarize the current status of interventional EUS in the treatment of esophageal and gastric varices and clarify the potential applications of this procedure.
INTERVENTIONAL EUS IN THE TREATMENT OF ESOPHAGEAL VARICES In 2000, Lahoti et al.14 first reported EUS-guided treatment of GI varices for 5
esophageal varices patients. In this small pilot study, EUS-guided injection sclerotherapy (EUS-EIS) was performed by injecting sclerosant (solium morrhuate) under real-time EUS guidance using a curved linear-array echoendoscope. The procedure involved injecting a sclerosant into the feeding vein (perforating vein) until no flow was detected by color Doppler EUS images. The sclerosant was injected at a rate of 2-4 mL per injection and 2.2 sessions per patient (range 2-3 sessions) were required to successfully obliterate the varices. One patient developed esophageal stenosis. No recurrent variceal bleeding occurred during the mean 15-month follow-up period (range 6-23 months). De Paulo et al.15 reported a randomized controlled trial of conventional EIS versus 5
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EUS-EIS treating 48 patients with esophageal varices. They made a hypothesis that obliteration of collateral veins would reduce the risk of recurrent bleeding, because recurrent variceal bleeding after endoscopic therapy is related to the presence of collateral veins.16-18 Twenty-four patients were treated with EIS using 3-5mL of 2.5%
ethanolamine oleate (EO) (diluted in 50% glucose) injected per injection. Up to 20 mL of EO was injected in each session. Another 24 patients were treated with EUS-EIS. The collateral veins were punctured under EUS guidance, and EO was injected as well. These procedures applied to both groups were repeated at 2-week intervals until the varices were obliterated. At the end of the treatment, there was no difference between the two groups in the number of procedures required to obliterate the varices (4.3 sessions in the EIS group; 4.1 sessions in the EUS-EIS group) or the total dose of sclerosant, and only minor differences in the number of complications (8.3% chest pain and 16.7 % bleeding in the EIS group; 16.7% chest pain and 4.2% bleeding in the EUS-EIS group). Eight patients (33.3%) continued to exhibit collateral veins after the treatment in the EIS group, whereas no patients in the EUS-EIS group continued to exhibit this condition. Four patients (16.7%) in the EIS group and 2 (8.3%) in the EUS-EIS group experienced variceal recurrence without recurrent bleeding during the follow-up period of at least six months (mean 22.6 months). More recently, Cameron et al.19 reported their experience of performing
EUS-guided CA injection of esophageal varices in their review article. 6
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INTERVENTIONAL EUS IN THE TREATMENT OF GASTRIC VARICES In 2007, Romero-Castro et al.20 first reported on the EUS-guided treatment of gastric varices. Five patients with gastric varices received EUS-guided CA injection using a curved
linear-array
echoendoscope.
A
1
mL
mixture
(1:1)
of
CA
(N-butyl-2-cyanoacrtlate; Histoacyl or Glubran2) plus lipiodol was injected into the varices at the entrance of the feeding veins (perforating veins) (Table 1). In cases in which the gastric varices were not completely obliterated, a further 1 mL CA-lipiodol mixture injection was performed a week after the initial procedure until variceal obliteration was achieved (Table 1). However, there was concern about the risk of CA migration21-23 even when employing EUS-guided treatment. Accordingly, some endoscopists chose EUS-guided coil deployment into the gastric varices in order to prevent the incidence of CA migration from occurring. EUS-guided coil deployment into of GI varices was first reported by Levy et al.24 for bleeding ectopic choledochojejunal anastmotic varices. Romero-Castro et al.25 first reported EUS-guided
coil deployment into gastric varices for four patients (Table 1). They inserted coils into the feeding veins (perforating veins) through 19-gauge injection needles to block the blood flow. The coils selected for EUS guided treatment were larger than 120% of the
measured diameter of the feeding veins (Table 2).
7
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Binmoeller et al.26 reported EUS-guided coil deployment and CA injection of
gastric varices, based on their successful application27 in the case of a bleeding gastric
varices patient for whom attempts to stop bleeding from varices by conventional endoscopic CA injection were unsuccessful. They hypothesized that a coil inserted into the varices prior to CA injection would function as a barrier to prevent CA from migrating into the larger veins causing embolic events. In their procedure, after visualizing the gastric varices from the esophagus through the diaphragmatic crus muscle under EUS guidance, a saline solution-primed 19-gauge FNA needle was inserted through the distal esophageal wall and diaphragm muscle directly into the gastric varices (Fig. 1).19,26 Then, coils were deployed and the injection of 1 mL of an undiluted ocrilate CA (2-ostyl-cyanoacylate; Dermabond) solution was performed, followed by 1 mL of saline flushing into the needle lumen to prevent CA occlusion (Fig. 2).19,26 This procedure was repeated immediately as needed until the varices were obliterated. One patient experienced recurrent bleeding from gastric varices 21 days after the procedure. Apart from that patient, 95.8% eradication of varices was achieved among 24 patients who were followed up for more than 6 months (Table 1, Fig. 3). Romero-Castro et al.28 subsequently conducted a multicenter trial of
EUS-guided coil deployment (EUS-Coiling) versus EUS-guided CA injection (EUS-CA) for 30 gastric varices patients. In this trial, EUS-Coiling was primary favored over EUS-CA, because they considered that the risks of coil migration and 8
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pulmonary coil embolism were very low. In cases where the accessibility of the feeding veins (perforating veins) was limited or the endosonographer found it too difficult to deploy a coil in the varix under EUS guidance, EUS-CA was chosen. All patients had a thoracic CT scan immediately after the procedure in order to check the pulmonary embolism and migration. One mL of a mixture (1:1) of N-butyl-2 cyanoacrylate (Histoacyl) and lipiodol was used for EUS-CA. To minimize the risk of pulmonary CA embolism, the CA dose was limited to 1 mL per session. In EUS-Coiling, the size of the coil chosen was larger than 120% of the varix diameter measured using EUS (Table 2). One week after the procedure, EUS was performed in all patients to check the variceal lumen. If the blood flow remained in the varix, the initial procedure was repeated until obliteration was achieved. A single session of coil application resulted in complete obliteration of the feeding veins (perforating veins) in 81.8% (9/11) in the EUS-Coiling group, and of 52.6% (10/19) in the EUS-CA group. Complications occurred in 1 patient (9.1%; 1/11, bleeding from esophageal varices) in the EUS-Coiling group and in 11
patients (57.9%; 11/19) in the EUS-CA group (Table 1). In the EUS-CA group, one patient had a fever and one had chest pain without pulmonary embolism on CT scan. However, nine (47.4%; 9/19) cases of asymptomatic pulmonary CA embolism were confirmed via CT scan in the EUS-CA group.
DISCUSSION 9
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Lahoti et al.14 and de Paulo et al.15 reported performing EUS-EIS into the feeding veins connected with the esophageal varices. Cameron et al.19 described the experience of performing EUS-CA on esophageal varices. However, we have to conclude that the clinical application of EUS-EIS to esophageal varices can be extremely limited in clinical settings because conventional endoscopic treatments such as EIS and EVL have achieved high success rates of esophageal variceal eradication3,5-8 and sclerosant injection into the feeding vein carries the risk of leakage into the greater circulatory system including such as the heart or lungs. Romero-Castro et al.20,25,28 and Binmoeller et al.26 have reported on the high
eradication rate and fewer complications achieved by EUS-guided treatment of gastric varices using CA, coil, and CA plus coil (Table 1). If the lumen of a gastric varix is large (e.g., 10 mm or larger), EUS-guide treatment may be useful for experienced endosonographers who are knowledgeable in the treatment of gastric varices. Regarding the procedure, EUS-CA carries a high risk of pulmonary CA embolization or migration, whereas EUS-Coiling carries only a very small risk of these complications occurring. Accordingly, we think EUS-Coiling is more acceptable than EUS-CA. However, with regard to EUS-Coiling for gastric varices, some problems remain to be solved. In terms of the cost for successful obliteration of gastric varices, Romero-Castro et al.28 showed that treatment with coils (mean cost 578.50 US dollars) costs significantly more than treatment with CA (mean cost 198.60 US dollars). They also described EUS-Coiling as 10
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being generally regarded as technically more demanding than EUS-CA.28 This is
because in EUS-CA we puncture the varices and inject 1mL of CA into the varices with a 22 G needle, while in EUS-Coiling we have to puncture the varices with a 19 G needle and then deploy coils using a pusher to keep them in place until blood flow in the varices is not observed. Romero-Castro et al.20,25,28 and Binmoeller et al.26 employed a 19-gauge FNA needle to deploy coils using an EUS-guide and large diameter coils.
However, Levy et al.29 mentioned in their review that they prefer a 22-gauge needle rather than a 19-gauge needle and that they prefer smaller and often shorter coils because of their ease of use and low potential risk of acute bleeding at the puncture site (Table 2). The coil size and needle gauge selected depend on the size of the varices measured using EUS. If the varices are larger, it is necessary to select larger coils and a larger needle to prevent coil migration. Moreover, it is also necessary to establish a consensus on an appropriate pusher (a guide wire or a stylet), a suitable site for injection (a varix or a perforating vein) and an application procedure for the combined use of CA or sclerosants with a coil. In conclusion, interventional EUS has a number of potential applications in the
treatment of gastric varices using coil deployment. However, since interventional EUS is carried out in a limited number of institutions around the world, a prospective multi-center worldwide study should be conducted to clarify the true clinical applicability of this procedure and establish a treatment strategy. 11
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ACKNOWLEDGMENT We wish to express my deep appreciation for Rei Suzuki and Kazuko Abe for their contribution in proofreading this paper and also express our gratitude to Tadayuki Takagi, Ko Watanabe, Jun Nakamura, Mitsuru Sugimoto, Naoki Konno, Yuichi Waragai, Hitomi Kikuchi, and Mika Takasumi for their collaboration in the endoscopic treatment for GI varices patients, and to all the endoscopy medical staff involved for their cooperation in the assistance of endoscopic procedures, including interventional EUS and EIS. We would also like to thank Takuji Gotoda and Kenichi Goda for reviewing this paper.
CONFLICT OF INTERESTS The authors declare that they have no conflict of interests concerning this article.
12
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2. Kim T, Shinjo H, Kokawa H, et al. Risk factors for hemorrhage from gastric fundal varices. Hepatology 1997; 25: 307-12.
3. Iso Y, Kawanaka H, Tomikawa M, et al. Repeated injection sclerotherapy is preferable to combined therapy with variceal ligation to avoid recurrence of esophageal varices: a prospective randomized trial. Hepatogastroenterol 1997; 44:
467-71.
4. Kanagawa H, Mima S, Kouyama H, Gotoh K, Uchida T, Okuda K. Treatment of gastric fundal varices by balloon-occluded retrograde transvenous obliteration. J
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5. Eisen GM, Baron TH, Dominitz JA, et al. The role of endoscopic therapy in the management of variceal hemorrahage. Gastrointest Endosc 2002; 56: 618-20.
6. Van Stiegmann G, Cambre T, Sun JH. A new endoscopic elastic band ligating device. Gastrointest Endosc 1986; 32: 230-3.
7. Hou MC, Lin HC, Lee FY, Chang FY, Lee SD. Recurrence of esophageal varices following endoscopic treatment and its impact on rebleeding: comparison of sclerotherapy and ligation. J Hepatol 2000; 32: 202-8.
8. Sarin SK, Govil A, Jain AK, et al. Prospective randomized trial of endoscopic 13
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sclerotherapy versus variceal band ligation for esophageal varices: influence on gastropathy, gastric varices and variceal recurrence. J Hepatol 1997; 26: 826-32.
9. Huang YH, Yeh HZ, Chen GH, et al. Endoscopic treatment of bleeding gastric varices by N-butyl-2-cyanoacrylate (Histoacryl) injection: long-term efficacy and safety. Gastrointest Endosc 2000; 52: 160-7.
10. Vilmann P, Jacobsen GK, Henriksen FW, Hancke S. Endoscopic ultrasonography with guided fine needle aspiration biopsy in pancreatic disease. Gastrointest Endosc 1992; 38: 172-3.
11. Hikichi T, Irisawa A, Bhutani MS, et al. Endoscopic ultrasound-guided fine-needle aspiration of solid pancreatic masses with rapid on-site cytological evaluation by endosonographers without attendance of cytopathologists. J Gastroenterol 2009; 44: 322-8.
12. Wakatsuki T, Irisawa A, Bhutani MS, et al. A comparative study of diagnostic value of cytologic sampling by endoscopic ultrasonography-guided fine-needle aspiration and that by endoscopic retrograde pancreatography for the management of pancreatic masses without biliary stricture. J Gastroenterol Hepatol 2005; 20:
1701-11.
13. Hikichi T, Irisawa A, Takagi T, et al. A case of transgastric gallbladder puncture as a complication during endoscopic ultrasound-guided drainage of a pancreatic pseudocyst. Fukushima J Med Sci 2007; 53: 11-9. 14
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14. Lahoti S, Catalano MF, Alcocer E, Hogan WJ, Geenen JE. Obliteration of esophageal varices using EUS-guided sclerotherapy with color Doppler. Gastrointest Endosc 2000; 51: 331-3.
15. De Paulo GA, Ardengh JC, Nakao FS, Ferrari AP. 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.
16. 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: 374-80.
17. 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.
18. Irisawa A, Obara K, Bhutani MS, et al. Role of para-esophageal collateral veins in patients with portal hypertension based on the results of endoscopic ultrasonography and liver scintigraphy analysis. J Gastroenterol Hepatol 2003; 18: 309-14.
19. Cameron R, Binmoeller KF. Cyanoacrylate applications in the GI tract. Gastrointest Endosc 2013; 77: 846-57.
20. Romero-Castro R, Pellicer-Bautista FJ, Jimenez-Saenz M, et al. EUS-guided 15
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injection of cyanoacrylate in perforating feeding veins in gastric varices: results in 5 cases. Gastrointest Endosc 2007; 66: 402-7.
21. Palejwala AA, Smart HL, Hughes M. Multiple pulmonary glue emboli following gastric variceal obliteration. Endoscopy 2000; 32: S1-2.
22. Tan YM, Goh KL, Kamarulzaman A, et al. Multiple systemic embolisms with septicemia after gastric variceal obliteration with cyanoacrylate. Gastrointest Endosc 2002; 55: 276-8.
23. Saracco G, Giordanino C, Roberto N, et al. Fatal multiple systemic embolisms after injection of cyanoacrylate in bleeding gastric varices of a patient who was noncirrhotic but with idiopathic portal hypertension. Gastrointest Endosc 2007; 65: 345-7.
24. Levy MJ, Wong Kee Song LM, Kendrick ML, Misra S, Gostout CJ. EUS-guided coil embolization for refractory ectopic variceal bleeding (with videos). Gastrointest Endosc 2008; 67: 572-4.
25. Romero-Castro R, Pellicer-Bautista F, Giovannini M, et al. Endoscopic ultrasound (EUS) - guided coil embolization therapy in gastric varices. Endoscopy 2010; 42: E35-6.
26. Binmoeller KF, Weilert F, Shah JN, Kim J. EUS-guided transesophageal treatment of gastric fundal varices with combined coiling and cyanoacrylate glue injection (with videos). Gastrointest Endosc 2011; 74: 1019-25. 16
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27. Sanchez-Yague A, Shah JN, Nguyen-Tag T, et al. EUS-guided coil embolization of gastric varices after unsuccessful endoscopic glue injection [abstract]. Gastrointest Endosc 2009; 69: AB6.
28. Romero-Castro R, Ellrichmann M, Ortiz-Maoyano C, et al. EUS-guided coil versus cyanoacrylate therapy for the treatment of gastric varices: a multicenter study (with videos). Gastrointest Endosc 2013; 78: 711-21.
29. Levy MJ, Wong Kee Song LM. EUS-guided angiotherapy for gastric varices: coil, glue, and sticky issues. Gastrointest Endosc 2013; 78: 722-5.
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FIGURE LEGENDS Figure 1. Transesophageal-transcrural approach to gastric varices. (a) Anatomic diagram. (b) EUS view. The yellow dashed line is the direction of the injection needle. V, gastic varix. (Reprinted from Gastrointest Endosc, Cameron R, Binmoeller KF. Cyanoacrylate applications in the GI tract. 2013; 77: 846-57 in reference [19] with permission from Elsevier).
Figure 2. Procedure of EUS-guided treatment of gastric varices with combined coiling and cyanoacrylate glue (CA) injection. (a) Transesophageal EUS views (Forward-view curved-linear array echoencoscpe) showing gastric varix targeted with a 19-gauge needle (arrow). (b) Deployment of coil (arrows) through the 19-gauge needle, (c) Injection of 1 mL of CA through the 19-gauge needle to obliterate the varix lumen. (d) Eradication of gastric varices (conventional curved linear echoendoscope). C, crus muscle; F, gastric fundus; MP, muscularis propria of the stomach wall. (Reprinted from Gastrointest Endosc, Binmoeller KF, Weilert F, Shah JN, Kim J. EUS-guided transesophageal treatment of gastric fundal varices with combined coiling and cyanoacrylate glue injection. 2011; 74: 1019-25 in reference [26] with permission from Elsevier).
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Figure 3. Obliteration of gastric varices by using coils and cyanoacrylate glue (CA). (a) Gastric varices in a conventional endoscopic view. (b) EUS-guided injection of coil followed by injection 1 mL of CA. (c) Extravasation of coil from obliterated varix 6 weeks later. (d) Varices eradicated at 1-year follow-up. (Reprinted from Gastrointest
Endosc, Cameron R, Binmoeller KF. Cyanoacrylate applications in the GI tract. 2013; 77: 846-57 in reference [19] with permission from Elsevier).
19
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FIGURES Figure 1
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Figure 2
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Figure 3
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Table 1. EUS-guided treatment for gastric varices Injected
Author
Romero-Castr
Obliteration rate
Recurrent GV bleeding
Complication
% (n)
rate % (n)
% (n)
No. of Pt materials
CA
5
100% (5/5)
0% (0/5)
o et al.20
Romero-Castr
0% (0/5)
(mean 10M, range 4-16)
Coil
4
75% (3/4)
0% (0/4)
o et al.25
0% (0/4)
(mean 5M, range 1-13)
Binmoeller KF
Coil
et al.26
CA
Romero-Castr
Coil
o et al.28
CA
and
or
30
95.8% (23/24)
4.2% (1/24)
(mean 193D, range
(mean
24-589)
24-589)
in
90.9% (10/11) in
0% (0/30)
coil, 19 in
coil, 100% (19/19)
(mean
CA
in CA
6-41)
30;
11
193D,
17.2M,
0% (0/30)
range
9.1% (1/11) in coil (1 bleeding
range
from
esophageal
varices),
57.9%
(11/19)
CA
in
(9
asymptomatic pulmonary CA
embolism detected by CT, 1
fever, 1 chest pain)
Pt, patient; GV, gastric varix; CA, cyanoacrylate; M, months; D, days; CT, computed tomography
23
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Table 2. Devices used by EUS-guided coil deployment for gastric varices Coil
Author
Needle size
Pusher
Diameter
Lengths
Romero-Castro et al.25
8-15mm
50-150mm
19G
0.035 inch GW
Binmoeller KF et al.26
12-20mm
Not shown
19G
FNA needle stylet
Romero-Castro et al.28
8-20mm
50-150mm
19G
0.035 inch GW
Levy et al.29
6-10mm
70-140mm
22G
FNA needle stylet
G, gauge; GW, guide wire
24
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1
Review
Potential application of interventional endoscopic ultrasonography for the treatment of esophageal and gastric varices1
Takuto Hikichi1, Katsutoshi Obara1, Shin-ichi Nakamura2, Atsushi Irisawa3, and Hiromasa Ohira4
1
Department of Endoscopy, Fukushima Medical University Hospital, Fukushima, Japan,
2
Department of Gastroenterology, Tokyo Women’s Medical University Hospital, Tokyo,
Japan, 3Department of Gastroenterology, Fukushima Medical University Aizu Medical
Center, Aizuwakamatsu, Japan, 4Department of Gastroenterology and Rheumatology, Fukushima Medical University School of Medicine, Fukushima, Japan.
Running title: Interventional EUS for GI varices
Correspondence: Takuto Hikichi, MD, PhD,
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/den.12436
1
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2
Associate Professor, Department of Endoscopy, Fukushima Medical University Hospital, 1 Hikarigaoka, Fukushima city, Fukushima, 960-1295, Japan Tel: +81-24-547-1583, Fax: +81-24-547-1586, Email: [email protected]
2
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Abstract
Interventional endoscopic ultrasonography (EUS) has been developed mainly for the treatment of pancreatico-biliary disorders (e.g., cyst drainage for pancreatic pseudocysts, biliary drainage for malignant biliary obstruction, and celiac plexus neurolysis). Recently, the application of interventional EUS has been expanded to a new field, the treatment of gastrointestinal varices. There have been several studies examining this new technique for the treatment of esophageal and gastric varices. In this review, we have aimed to summarize the current status of interventional EUS for the treatment of esophageal and gastric varices (e.g., EUS-guided coil deployment for gastric varices) and to clarify the clinical feasibility of this procedure.
Key words: coil, cyanoacrylate, endoscopic ultrasonography (EUS), interventional EUS, varix
3
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4
INTRODUCTION Bleeding from esophageal and gastric varices often causes catastrophic
hemodynamic deterioration and is one of the most common causes of death among patients with portal hypertension such as those suffering from liver cirrhosis. Therefore, the successful treatment of bleeding esophageal and gastric varices can significantly improve the outcome for such patients.1-9 Varices that are large and/or red color sign are considered to be at high risk of bleeding and are treated prophylactically by endoscopic1-3 or interventional radiology (IVR)4 therapy. There are two types of endoscopic treatment for esophageal varices, namely endoscopic injection sclerothrapy (EIS) using sclerosants5 and endoscopic variceal ligation (EVL).6 Regarding gastric varices with large variceal lumen and rapid blood flow, cyanoacylate glue (CA) injection1,9 under conventional endoscopy has been the first choice treatment especially in cases of bleeding. However, conventional endoscopic approach is “blind.” Because we cannot see directly the depth of the varix, we sometimes cannot inject CA or sclerosants into the varices. IVR therapy such as balloon-occluded retrograde transvenous obliteration (B-RTO)4 has been performed for prophylactic gastric varices cases. However, a large volume of sclerosant is required and the catheter must remain in position for several hours in order to perform B-RTO. Interventional endoscopic ultrasonography (EUS), including EUS-guided fine
needle aspiration, was developed by Vilmann et al.10 in 1992 and has been popular in the 4
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5
diagnosis of pancreatic tumors,11,12 gastrointestinal (GI) subepithelial tumors, pancreatic
pseudocyst drainage,13 celiac plexus neurolysis, and other procedures. Recently, several studies utilized the interventional EUS technique in the treatment of GI varices. The biggest advantage of interventional EUS is that it allows the surgeon to see the varix lumen directly in the real-time. Here, we summarize the current status of interventional EUS in the treatment of esophageal and gastric varices and clarify the potential applications of this procedure.
INTERVENTIONAL EUS IN THE TREATMENT OF ESOPHAGEAL VARICES In 2000, Lahoti et al.14 first reported EUS-guided treatment of GI varices for 5
esophageal varices patients. In this small pilot study, EUS-guided injection sclerotherapy (EUS-EIS) was performed by injecting sclerosant (solium morrhuate) under real-time EUS guidance using a curved linear-array echoendoscope. The procedure involved injecting a sclerosant into the feeding vein (perforating vein) until no flow was detected by color Doppler EUS images. The sclerosant was injected at a rate of 2-4 mL per injection and 2.2 sessions per patient (range 2-3 sessions) were required to successfully obliterate the varices. One patient developed esophageal stenosis. No recurrent variceal bleeding occurred during the mean 15-month follow-up period (range 6-23 months). De Paulo et al.15 reported a randomized controlled trial of conventional EIS versus 5
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EUS-EIS treating 48 patients with esophageal varices. They made a hypothesis that obliteration of collateral veins would reduce the risk of recurrent bleeding, because recurrent variceal bleeding after endoscopic therapy is related to the presence of collateral veins.16-18 Twenty-four patients were treated with EIS using 3-5mL of 2.5%
ethanolamine oleate (EO) (diluted in 50% glucose) injected per injection. Up to 20 mL of EO was injected in each session. Another 24 patients were treated with EUS-EIS. The collateral veins were punctured under EUS guidance, and EO was injected as well. These procedures applied to both groups were repeated at 2-week intervals until the varices were obliterated. At the end of the treatment, there was no difference between the two groups in the number of procedures required to obliterate the varices (4.3 sessions in the EIS group; 4.1 sessions in the EUS-EIS group) or the total dose of sclerosant, and only minor differences in the number of complications (8.3% chest pain and 16.7 % bleeding in the EIS group; 16.7% chest pain and 4.2% bleeding in the EUS-EIS group). Eight patients (33.3%) continued to exhibit collateral veins after the treatment in the EIS group, whereas no patients in the EUS-EIS group continued to exhibit this condition. Four patients (16.7%) in the EIS group and 2 (8.3%) in the EUS-EIS group experienced variceal recurrence without recurrent bleeding during the follow-up period of at least six months (mean 22.6 months). More recently, Cameron et al.19 reported their experience of performing
EUS-guided CA injection of esophageal varices in their review article. 6
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INTERVENTIONAL EUS IN THE TREATMENT OF GASTRIC VARICES In 2007, Romero-Castro et al.20 first reported on the EUS-guided treatment of gastric varices. Five patients with gastric varices received EUS-guided CA injection using a curved
linear-array
echoendoscope.
A
1
mL
mixture
(1:1)
of
CA
(N-butyl-2-cyanoacrtlate; Histoacyl or Glubran2) plus lipiodol was injected into the varices at the entrance of the feeding veins (perforating veins) (Table 1). In cases in which the gastric varices were not completely obliterated, a further 1 mL CA-lipiodol mixture injection was performed a week after the initial procedure until variceal obliteration was achieved (Table 1). However, there was concern about the risk of CA migration21-23 even when employing EUS-guided treatment. Accordingly, some endoscopists chose EUS-guided coil deployment into the gastric varices in order to prevent the incidence of CA migration from occurring. EUS-guided coil deployment into of GI varices was first reported by Levy et al.24 for bleeding ectopic choledochojejunal anastmotic varices. Romero-Castro et al.25 first reported EUS-guided
coil deployment into gastric varices for four patients (Table 1). They inserted coils into the feeding veins (perforating veins) through 19-gauge injection needles to block the blood flow. The coils selected for EUS guided treatment were larger than 120% of the
measured diameter of the feeding veins (Table 2).
7
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Binmoeller et al.26 reported EUS-guided coil deployment and CA injection of
gastric varices, based on their successful application27 in the case of a bleeding gastric
varices patient for whom attempts to stop bleeding from varices by conventional endoscopic CA injection were unsuccessful. They hypothesized that a coil inserted into the varices prior to CA injection would function as a barrier to prevent CA from migrating into the larger veins causing embolic events. In their procedure, after visualizing the gastric varices from the esophagus through the diaphragmatic crus muscle under EUS guidance, a saline solution-primed 19-gauge FNA needle was inserted through the distal esophageal wall and diaphragm muscle directly into the gastric varices (Fig. 1).19,26 Then, coils were deployed and the injection of 1 mL of an undiluted ocrilate CA (2-ostyl-cyanoacylate; Dermabond) solution was performed, followed by 1 mL of saline flushing into the needle lumen to prevent CA occlusion (Fig. 2).19,26 This procedure was repeated immediately as needed until the varices were obliterated. One patient experienced recurrent bleeding from gastric varices 21 days after the procedure. Apart from that patient, 95.8% eradication of varices was achieved among 24 patients who were followed up for more than 6 months (Table 1, Fig. 3). Romero-Castro et al.28 subsequently conducted a multicenter trial of
EUS-guided coil deployment (EUS-Coiling) versus EUS-guided CA injection (EUS-CA) for 30 gastric varices patients. In this trial, EUS-Coiling was primary favored over EUS-CA, because they considered that the risks of coil migration and 8
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pulmonary coil embolism were very low. In cases where the accessibility of the feeding veins (perforating veins) was limited or the endosonographer found it too difficult to deploy a coil in the varix under EUS guidance, EUS-CA was chosen. All patients had a thoracic CT scan immediately after the procedure in order to check the pulmonary embolism and migration. One mL of a mixture (1:1) of N-butyl-2 cyanoacrylate (Histoacyl) and lipiodol was used for EUS-CA. To minimize the risk of pulmonary CA embolism, the CA dose was limited to 1 mL per session. In EUS-Coiling, the size of the coil chosen was larger than 120% of the varix diameter measured using EUS (Table 2). One week after the procedure, EUS was performed in all patients to check the variceal lumen. If the blood flow remained in the varix, the initial procedure was repeated until obliteration was achieved. A single session of coil application resulted in complete obliteration of the feeding veins (perforating veins) in 81.8% (9/11) in the EUS-Coiling group, and of 52.6% (10/19) in the EUS-CA group. Complications occurred in 1 patient (9.1%; 1/11, bleeding from esophageal varices) in the EUS-Coiling group and in 11
patients (57.9%; 11/19) in the EUS-CA group (Table 1). In the EUS-CA group, one patient had a fever and one had chest pain without pulmonary embolism on CT scan. However, nine (47.4%; 9/19) cases of asymptomatic pulmonary CA embolism were confirmed via CT scan in the EUS-CA group.
DISCUSSION 9
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Lahoti et al.14 and de Paulo et al.15 reported performing EUS-EIS into the feeding veins connected with the esophageal varices. Cameron et al.19 described the experience of performing EUS-CA on esophageal varices. However, we have to conclude that the clinical application of EUS-EIS to esophageal varices can be extremely limited in clinical settings because conventional endoscopic treatments such as EIS and EVL have achieved high success rates of esophageal variceal eradication3,5-8 and sclerosant injection into the feeding vein carries the risk of leakage into the greater circulatory system including such as the heart or lungs. Romero-Castro et al.20,25,28 and Binmoeller et al.26 have reported on the high
eradication rate and fewer complications achieved by EUS-guided treatment of gastric varices using CA, coil, and CA plus coil (Table 1). If the lumen of a gastric varix is large (e.g., 10 mm or larger), EUS-guide treatment may be useful for experienced endosonographers who are knowledgeable in the treatment of gastric varices. Regarding the procedure, EUS-CA carries a high risk of pulmonary CA embolization or migration, whereas EUS-Coiling carries only a very small risk of these complications occurring. Accordingly, we think EUS-Coiling is more acceptable than EUS-CA. However, with regard to EUS-Coiling for gastric varices, some problems remain to be solved. In terms of the cost for successful obliteration of gastric varices, Romero-Castro et al.28 showed that treatment with coils (mean cost 578.50 US dollars) costs significantly more than treatment with CA (mean cost 198.60 US dollars). They also described EUS-Coiling as 10
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being generally regarded as technically more demanding than EUS-CA.28 This is
because in EUS-CA we puncture the varices and inject 1mL of CA into the varices with a 22 G needle, while in EUS-Coiling we have to puncture the varices with a 19 G needle and then deploy coils using a pusher to keep them in place until blood flow in the varices is not observed. Romero-Castro et al.20,25,28 and Binmoeller et al.26 employed a 19-gauge FNA needle to deploy coils using an EUS-guide and large diameter coils.
However, Levy et al.29 mentioned in their review that they prefer a 22-gauge needle rather than a 19-gauge needle and that they prefer smaller and often shorter coils because of their ease of use and low potential risk of acute bleeding at the puncture site (Table 2). The coil size and needle gauge selected depend on the size of the varices measured using EUS. If the varices are larger, it is necessary to select larger coils and a larger needle to prevent coil migration. Moreover, it is also necessary to establish a consensus on an appropriate pusher (a guide wire or a stylet), a suitable site for injection (a varix or a perforating vein) and an application procedure for the combined use of CA or sclerosants with a coil. In conclusion, interventional EUS has a number of potential applications in the
treatment of gastric varices using coil deployment. However, since interventional EUS is carried out in a limited number of institutions around the world, a prospective multi-center worldwide study should be conducted to clarify the true clinical applicability of this procedure and establish a treatment strategy. 11
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ACKNOWLEDGMENT We wish to express my deep appreciation for Rei Suzuki and Kazuko Abe for their contribution in proofreading this paper and also express our gratitude to Tadayuki Takagi, Ko Watanabe, Jun Nakamura, Mitsuru Sugimoto, Naoki Konno, Yuichi Waragai, Hitomi Kikuchi, and Mika Takasumi for their collaboration in the endoscopic treatment for GI varices patients, and to all the endoscopy medical staff involved for their cooperation in the assistance of endoscopic procedures, including interventional EUS and EIS. We would also like to thank Takuji Gotoda and Kenichi Goda for reviewing this paper.
CONFLICT OF INTERESTS The authors declare that they have no conflict of interests concerning this article.
12
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8. Sarin SK, Govil A, Jain AK, et al. Prospective randomized trial of endoscopic 13
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sclerotherapy versus variceal band ligation for esophageal varices: influence on gastropathy, gastric varices and variceal recurrence. J Hepatol 1997; 26: 826-32.
9. Huang YH, Yeh HZ, Chen GH, et al. Endoscopic treatment of bleeding gastric varices by N-butyl-2-cyanoacrylate (Histoacryl) injection: long-term efficacy and safety. Gastrointest Endosc 2000; 52: 160-7.
10. Vilmann P, Jacobsen GK, Henriksen FW, Hancke S. Endoscopic ultrasonography with guided fine needle aspiration biopsy in pancreatic disease. Gastrointest Endosc 1992; 38: 172-3.
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12. Wakatsuki T, Irisawa A, Bhutani MS, et al. A comparative study of diagnostic value of cytologic sampling by endoscopic ultrasonography-guided fine-needle aspiration and that by endoscopic retrograde pancreatography for the management of pancreatic masses without biliary stricture. J Gastroenterol Hepatol 2005; 20:
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13. Hikichi T, Irisawa A, Takagi T, et al. A case of transgastric gallbladder puncture as a complication during endoscopic ultrasound-guided drainage of a pancreatic pseudocyst. Fukushima J Med Sci 2007; 53: 11-9. 14
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14. Lahoti S, Catalano MF, Alcocer E, Hogan WJ, Geenen JE. Obliteration of esophageal varices using EUS-guided sclerotherapy with color Doppler. Gastrointest Endosc 2000; 51: 331-3.
15. De Paulo GA, Ardengh JC, Nakao FS, Ferrari AP. 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.
16. 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: 374-80.
17. 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.
18. Irisawa A, Obara K, Bhutani MS, et al. Role of para-esophageal collateral veins in patients with portal hypertension based on the results of endoscopic ultrasonography and liver scintigraphy analysis. J Gastroenterol Hepatol 2003; 18: 309-14.
19. Cameron R, Binmoeller KF. Cyanoacrylate applications in the GI tract. Gastrointest Endosc 2013; 77: 846-57.
20. Romero-Castro R, Pellicer-Bautista FJ, Jimenez-Saenz M, et al. EUS-guided 15
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injection of cyanoacrylate in perforating feeding veins in gastric varices: results in 5 cases. Gastrointest Endosc 2007; 66: 402-7.
21. Palejwala AA, Smart HL, Hughes M. Multiple pulmonary glue emboli following gastric variceal obliteration. Endoscopy 2000; 32: S1-2.
22. Tan YM, Goh KL, Kamarulzaman A, et al. Multiple systemic embolisms with septicemia after gastric variceal obliteration with cyanoacrylate. Gastrointest Endosc 2002; 55: 276-8.
23. Saracco G, Giordanino C, Roberto N, et al. Fatal multiple systemic embolisms after injection of cyanoacrylate in bleeding gastric varices of a patient who was noncirrhotic but with idiopathic portal hypertension. Gastrointest Endosc 2007; 65: 345-7.
24. Levy MJ, Wong Kee Song LM, Kendrick ML, Misra S, Gostout CJ. EUS-guided coil embolization for refractory ectopic variceal bleeding (with videos). Gastrointest Endosc 2008; 67: 572-4.
25. Romero-Castro R, Pellicer-Bautista F, Giovannini M, et al. Endoscopic ultrasound (EUS) - guided coil embolization therapy in gastric varices. Endoscopy 2010; 42: E35-6.
26. Binmoeller KF, Weilert F, Shah JN, Kim J. EUS-guided transesophageal treatment of gastric fundal varices with combined coiling and cyanoacrylate glue injection (with videos). Gastrointest Endosc 2011; 74: 1019-25. 16
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27. Sanchez-Yague A, Shah JN, Nguyen-Tag T, et al. EUS-guided coil embolization of gastric varices after unsuccessful endoscopic glue injection [abstract]. Gastrointest Endosc 2009; 69: AB6.
28. Romero-Castro R, Ellrichmann M, Ortiz-Maoyano C, et al. EUS-guided coil versus cyanoacrylate therapy for the treatment of gastric varices: a multicenter study (with videos). Gastrointest Endosc 2013; 78: 711-21.
29. Levy MJ, Wong Kee Song LM. EUS-guided angiotherapy for gastric varices: coil, glue, and sticky issues. Gastrointest Endosc 2013; 78: 722-5.
17
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FIGURE LEGENDS Figure 1. Transesophageal-transcrural approach to gastric varices. (a) Anatomic diagram. (b) EUS view. The yellow dashed line is the direction of the injection needle. V, gastic varix. (Reprinted from Gastrointest Endosc, Cameron R, Binmoeller KF. Cyanoacrylate applications in the GI tract. 2013; 77: 846-57 in reference [19] with permission from Elsevier).
Figure 2. Procedure of EUS-guided treatment of gastric varices with combined coiling and cyanoacrylate glue (CA) injection. (a) Transesophageal EUS views (Forward-view curved-linear array echoencoscpe) showing gastric varix targeted with a 19-gauge needle (arrow). (b) Deployment of coil (arrows) through the 19-gauge needle, (c) Injection of 1 mL of CA through the 19-gauge needle to obliterate the varix lumen. (d) Eradication of gastric varices (conventional curved linear echoendoscope). C, crus muscle; F, gastric fundus; MP, muscularis propria of the stomach wall. (Reprinted from Gastrointest Endosc, Binmoeller KF, Weilert F, Shah JN, Kim J. EUS-guided transesophageal treatment of gastric fundal varices with combined coiling and cyanoacrylate glue injection. 2011; 74: 1019-25 in reference [26] with permission from Elsevier).
18
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Figure 3. Obliteration of gastric varices by using coils and cyanoacrylate glue (CA). (a) Gastric varices in a conventional endoscopic view. (b) EUS-guided injection of coil followed by injection 1 mL of CA. (c) Extravasation of coil from obliterated varix 6 weeks later. (d) Varices eradicated at 1-year follow-up. (Reprinted from Gastrointest
Endosc, Cameron R, Binmoeller KF. Cyanoacrylate applications in the GI tract. 2013; 77: 846-57 in reference [19] with permission from Elsevier).
19
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FIGURES Figure 1
20
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Figure 2
21
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Figure 3
22
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Table 1. EUS-guided treatment for gastric varices Injected
Author
Romero-Castr
Obliteration rate
Recurrent GV bleeding
Complication
% (n)
rate % (n)
% (n)
No. of Pt materials
CA
5
100% (5/5)
0% (0/5)
o et al.20
Romero-Castr
0% (0/5)
(mean 10M, range 4-16)
Coil
4
75% (3/4)
0% (0/4)
o et al.25
0% (0/4)
(mean 5M, range 1-13)
Binmoeller KF
Coil
et al.26
CA
Romero-Castr
Coil
o et al.28
CA
and
or
30
95.8% (23/24)
4.2% (1/24)
(mean 193D, range
(mean
24-589)
24-589)
in
90.9% (10/11) in
0% (0/30)
coil, 19 in
coil, 100% (19/19)
(mean
CA
in CA
6-41)
30;
11
193D,
17.2M,
0% (0/30)
range
9.1% (1/11) in coil (1 bleeding
range
from
esophageal
varices),
57.9%
(11/19)
CA
in
(9
asymptomatic pulmonary CA
embolism detected by CT, 1
fever, 1 chest pain)
Pt, patient; GV, gastric varix; CA, cyanoacrylate; M, months; D, days; CT, computed tomography
23
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Table 2. Devices used by EUS-guided coil deployment for gastric varices Coil
Author
Needle size
Pusher
Diameter
Lengths
Romero-Castro et al.25
8-15mm
50-150mm
19G
0.035 inch GW
Binmoeller KF et al.26
12-20mm
Not shown
19G
FNA needle stylet
Romero-Castro et al.28
8-20mm
50-150mm
19G
0.035 inch GW
Levy et al.29
6-10mm
70-140mm
22G
FNA needle stylet
G, gauge; GW, guide wire
24
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