LIVER TRANSPLANTATION 15:1508-1513, 2009

ORIGINAL ARTICLE

Endoscopic Variceal Ligation for Primary

Prophylaxis of Esophageal Variceal
Hemorrhage in Pre–Liver Transplant Patients
Eu Jin Lim,1 Paul J. Gow,1 and Peter W. Angus1
1
Department of Gastroenterology and Hepatology, Austin Hospital, Heidelberg, Victoria, Australia

Endoscopic variceal ligation (EVL) is widely used to prevent esophageal variceal bleeding in patients with advanced cirrhosis.
However, the safety and efficacy of EVL in this setting have not been clearly established. This study included 300 adult patients
with cirrhosis on our liver transplant waitlist who underwent upper gastrointestinal endoscopy. Esophageal varices deemed to
be at high risk of bleeding were banded until eradication or transplantation. A retrospective review of patient notes and
endoscopy databases was undertaken, and the number of banding episodes, complications, and patient outcomes were
recorded. Forty-two of 300 patients presented with or had previous variceal bleeding prior to referral and were excluded from
the analysis. Of the remaining 258 patients, 101 underwent a total of 259 banding episodes (2.6 per patient) with a median
follow-up post-banding of 18.4 months per patient (a total of 150 patient years). Failed prophylaxis occurred in 2 patients (2%),
and there were 3 episodes (1.2%) of acute hematemesis from band-induced ulceration. One patient (1%) had mild esophageal
stricturing post-banding without dysphagia. Four of 36 patients (11%) previously found to have moderately sized or larger
varices that were not banded presented with hematemesis due to variceal bleeding and were subsequently banded. None of
the patients that received banding died because of bleeding or failed to receive a transplant as a result of banding
complications. This study shows that in liver transplant candidates, EVL is highly effective in preventing first variceal bleed.
Although banding carries a small risk of band-induced bleeding, this rate is low in comparison with the predicted rate of variceal
bleeding in this population. Liver Transpl 15:1508-1513, 2009. © 2009 AASLD.

Received February 22, 2009; accepted June 23, 2009.

Current guidelines recommend the use of either nonse- bleed5 as well as reducing bleeding-related and all-
lective beta-blockers or endoscopic variceal ligation cause mortality.6 However, EVL is associated with po-
(EVL) to prevent first variceal bleeding in patients at tential complications such as upper gastrointestinal
high risk.1 Nonselective beta-blockers reduce variceal bleeding from band-induced ulcers, esophageal perfo-
bleeding2 and overall mortality in patients with cirrho- ration, dysphagia due to scar-induced esophageal stric-
sis.3 However, patients with end-stage liver failure often ture, and the development of and bleeding from gastric
tolerate therapeutic doses of nonselective beta-blockers varices.
poorly because of the development of symptomatic bra- A recent study of patients on a liver transplant wait-
dycardia, hypotension, fatigue, or dyspnea. In addition, list revealed that 6.5% of 31 patients who underwent
about a third of patients will not achieve a reduction in prophylactic variceal banding bled from band-induced
portal pressures sufficient to prevent variceal bleeding esophageal ulcers, and this resulted in the death of 1
despite receiving therapeutic doses of beta-blockers.4 patient.7 However, another similarly sized study of liver
Because of these concerns, some units have routinely transplant candidates reported no banding-related
employed EVL as primary prophylaxis in preference to bleeding events and complete protection from variceal
beta-blockers for patients awaiting liver transplanta- bleeding.8 The widely differing results of these 2 studies
tion who are at high risk of variceal bleeding. EVL has may reflect the relatively small patient populations
been shown to be effective in reducing first variceal studied and/or differences in banding experience and

Abbreviations: EVL, endoscopic variceal ligation; MELD, Model for End-Stage Liver Disease; NIEC, North Italian Endoscopic Club.
Address reprint requests to Eu Jin Lim, Department of Gastroenterology and Hepatology, Austin Hospital, 145 Studley Road, Heidelberg, Victoria
3084, Australia. Telephone: 0403 327 841; E-mail: [email protected]
DOI 10.1002/lt.21857
Published online in Wiley InterScience (www.interscience.wiley.com).

© 2009 American Association for the Study of Liver Diseases.

 15276473, 2009, 11, Downloaded from https://aasldpubs.onlinelibrary.wiley.com/doi/10.1002/lt.21857 by EBMG ACCESS - GHANA, Wiley Online Library on [27/02/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
VARICEAL BANDING IN LIVER TRANSPLANT CANDIDATES 1509

technique. The aim of the current study, therefore, was

TABLE 1. North Italian Endoscopic Club Score
to evaluate the safety and efficacy of EVL as primary
prophylaxis of variceal bleeding in a large population of
Variable Points to Add
patients awaiting liver transplantation.
Child-Pugh class A 6.5
B 13.0
PATIENTS AND METHODS C 19.5
Size of varices Small 8.7
A retrospective audit was undertaken of adult patients
Medium 13.0
with chronic liver disease on the Victorian liver trans-
Large 19.5
plant waitlist from 1998 to 2008 who had undergone Red Wale markings Absent 3.2
screening upper gastrointestinal endoscopy as part of Mild 6.4
their liver transplant workup. Children (age ⬍ 18) and Moderate 9.6
patients with fulminant hepatic failure were excluded. Severe 12.8
Cirrhosis was diagnosed on liver biopsy histology. Data
on the patient’s age, diagnosis, and severity of liver
disease, as determined by the Child-Pugh score, were presented with variceal bleeding or had previous
collected. variceal banding done prior to referral to our unit and
At endoscopy, if esophageal varices were present, were excluded from the analysis. Two hundred and
they were graded from I to IV according to Conn’s clas- fifty-eight patients did not have a history of variceal
sification.9 The presence of red wale markings, cherry bleeding and underwent endoscopic surveillance and
red spots, gastric varices, and portal hypertensive gas- primary prophylaxis performed as outlined previously.
tropathy was also recorded. Patients with varices There were 186 males and 72 females with a median
deemed to be at high risk of bleeding [large varices age of 50.1 years (age range of 17-69), and they were
(grade IV) or medium varices (grade III) with red wale followed up for 275 patient years (mean of 12.7 months
marking or cherry red spots] underwent prospective per patient). The etiology of cirrhosis in our patient
EVL after informed consent was obtained. Each session cohort is listed in Table 2. Nearly half the patients had
was performed by an endoscopist experienced at EVL. hepatitis C, alcohol, or both as the cause for cirrhosis.
Either the endoscopist or an anesthetist provided seda- Nineteen patients also had hepatocellular carcinomas
tion. In each session, 1 band was applied to each col- (Table 2). Of the 258 patients, 205 (80%) had varices
umn of varices in the distal 5 cm of the esophagus, and (Fig. 1). One hundred seventy-seven patients (68.6%)
as many bands as possible were applied (the number received a liver transplant, 23 patients (8.9%) were re-
varied from 1 to 7). Initially, a single-band ligation de- moved from the waiting list, 22 patients (8.5%) died
vice was used, with or without the aid of an overtube, waiting for a transplant, and 36 patients (14%) re-
but later a multiple-band instrument became standard. mained on the waiting list.
Acid suppression treatment with a proton pump inhib-
itor was used routinely.
Outcome in Treated Patients
Repeat endoscopy with EVL was performed every 4 to One hundred and one patients with grade III or IV
6 weeks until the esophageal varices were eradicated, varices underwent prophylactic EVL with a total of 259
the varices became too small to band, or the patient banding episodes (mean of 2.56 episodes per patient).
underwent liver transplantation. Patients with no vari- These patients were followed up post-banding for a total
ces or small varices underwent annual screening en- of 150 patient years with a median follow-up of 18.4
doscopy. The number of banding episodes and the months per patient. Twenty-five of these patients (25%)
number of patients who had a variceal bleed despite were receiving propranolol therapy at the time of refer-
EVL (primary prophylaxis failure) were recorded. Com- ral, but only 15 (15%) received presumed therapeutic
plications from EVL, including gastrointestinal bleed- doses of 20 mg twice a day or greater. Eighty-one of
ing from band-induced ulcers, dysphagia, esophageal these patients (80.2%) had Child-Pugh C cirrhosis, and
perforation, enlargement of or bleeding from gastric the mean Child-Pugh score was 11.2 (Table 3). The
varices, and death, were noted. The North Italian En- mean Model for End-Stage Liver Disease score was 20.
doscopic Club (NIEC) score, which combines the sever- The mean NIEC index was 37.1, with 50 patients
ity of liver disease (by Child-Pugh score), the size of (49.5%) having an NIEC index of more than 40 (Table 4).
varices, and the presence of red wale markings to esti- Of the patients that underwent variceal band ligation,
mate the risk of variceal bleeding without prophylaxis, 35 (34.7%) had grade IV varices, and 66 (65.3%) had
was calculated for each patient (see Table 1).10 The grade III varices. Thirty-seven patients (36.6%) had
ethics committee of the institution approved the study mild portal hypertensive gastropathy, 42 (41.6%) had
protocol. moderate portal hypertensive gastropathy, and 5 (5%)
had severe portal hypertensive gastropathy.
There were 2 episodes of variceal bleeding (2% of
RESULTS patients) despite EVL, and this meant an overall bleed-
Three hundred patients with chronic liver disease were ing rate from varices of 1.3% per patient year of fol-
placed on the waiting list for liver transplantation be- low-up post-banding. Both occurred more than 2 weeks
tween 1998 and 2008. Forty-two of the 300 patients post-EVL, and no band-induced ulcers were seen at
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1510 LIM, GOW, AND ANGUS

TABLE 2. Etiology of Cirrhosis

Diagnosis Number of Patients Patients with Hepatocellular Carcinoma

Hepatitis C 64 (25.3%) 10
Alcohol 30 (11.8%) 1
Hepatitis C ⫹ alcohol 26 (10.2%) 0
Hepatitis B 27 (10.6%) 4
Nonalcoholic steatohepatitis 13 (5.2%) 2
Cryptogenic cirrhosis 26 (10.2%) 1
Primary sclerosing cholangitis 27 (10.6%) 0
Primary biliary cirrhosis 12 (4.7%) 1
Other 29 (11.4%) 0

at emergent endoscopy. All 3 patients required blood

transfusion, 2 required intensive care unit admission,
and 1 required intubation and inotropes. These pa-
tients subsequently underwent 4 to 6 further banding
sessions without further complications to eventually
eradicate their varices.
One patient (1%) had mild esophageal stricturing
post-banding but no dysphagia. There were no esoph-
ageal perforations. No patient developed gastric varices
post-banding. Eight patients who had gastric varices
underwent EVL of their esophageal varices without
subsequent obvious enlargement of or bleeding from
Figure 1. Patients who underwent endoscopic surveillance their gastric varices. None of the patients that received
for esophageal varices. banding died because of bleeding or failed to receive a
transplant as a result of EVL-associated complications.
emergent endoscopy. One patient, who had Child-Pugh
B cirrhosis and was not on propranolol, was initially Outcome in Untreated Patients
found to have 4 grade IV varices with red wale markings
(NIEC index of 30) that were banded and was booked to One hundred and fifty-seven patients had endoscopic
have repeat endoscopy in 4 weeks but re-presented 3 surveillance but did not undergo EVL. They had a mean
months later with acute hematemesis. This patient Child-Pugh score of 10.4 and a mean Model for End-
subsequently underwent 3 further banding sessions Stage Liver Disease score of 20. One hundred and four
without complications to achieve variceal eradication. of these patients had varices: 2 (1.9%) had grade IV
The other patient, who had Child-Pugh C cirrhosis and varices, 34 (32.7%) had grade III varices without red
was on propranolol (10 mg twice a day), was initially wale markings, and 69 (65.4%) had grade I or II varices.
found to have 3 grade III varices (NIEC index of 35.7) The 36 patients with grade III or larger varices had a
that were banded and presented at 4 weeks with acute mean NIEC index of 27.16 (predicted annual bleeding
hematemesis before repeat endoscopy could be done. rate of 22%) and were followed up for 35.6 patient
This patient subsequently underwent another 2 band- years. Four of these patients (11%) subsequently pre-
ing sessions without complications to achieve variceal sented with acute hematemesis due to variceal bleeding
eradication. The observed variceal bleeding rate with and were subsequently banded with a total of 13 band-
EVL intervention, compared to the predicted variceal ing episodes (mean of 3.25 episodes per patient). None
bleeding rate without intervention according to the of these patients had complications relating to EVL.
NIEC, is presented in Table 4. There were no variceal bleeds among the 68 patients
who had only grade I or II varices or among the 53
patients with no varices. With respect to pharmacolog-
Complications ical therapy, of the 157 patients who were not prophy-
Three patients (1.15% of banding episodes) had acute lactically banded, only 20 (12.7%) were on propranolol,
hematemesis from band-induced ulceration despite of whom only 11 (7%) were on doses of 20 mg twice a
routine proton pump inhibitor use. All 3 patients had day or greater.
Child-Pugh C cirrhosis with NIEC indices between 42.1
and 46.5. Only 1 of the 3 patients was on propranolol
(at a dose of 20 mg twice a day). Two of the patients had
DISCUSSION
3 grade III varices with red wale markings, and 1 patient In the absence of prophylaxis, 50% of Child-Pugh C
had 2 grade IV varices with red wale markings. All patients with cirrhosis will suffer a variceal hemorrhage
bleeding episodes occurred within 2 weeks of the first after 1 year,11 and this is associated with an in-patient
banding session, and band-induced ulcers were noted mortality rate of at least 20%.12 Although primary pro-
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VARICEAL BANDING IN LIVER TRANSPLANT CANDIDATES 1511

TABLE 3. Child-Pugh Scores of Candidates for Primary Prophylaxis

Patients Banded Patients Not Banded

Child-Pugh class A 3 (3.0%) 19 (12.1%)
B 17 (16.8%) 41 (26.1%)
C 81 (80.2%) 97 (61.8)
Mean Child-Pugh score 11.2 10.4
Mean MELD Score 20 20

Abbreviation: MELD, Model for End-Stage Liver Disease.

TABLE 4. NIEC Scores in Patients Undergoing Endoscopic Variceal Ligation

Number of Predicted Annual Observed Annual

Risk NIEC Patients Bleeding Risk Bleeding Rate (With
Class Index Banded (Without Intervention) Intervention)
1 ⬍ 20 6 (5.9%) 9.5% 0%
2 20-25 5 (5.0%) 15.8% 0%
3 25.1-30 8 (7.9%) 22.2% 12.5%
4 30.1-35 0 (0%) 32.1% 0%
5 35.1-40 31 (30.7%) 50.0% 2.71%
6 ⬎ 40 50 (49.5%) 63.6% 0%

Abbreviation: NIEC, North Italian Endoscopic Club.

phylaxis with EVL has been shown to reduce the risk of group were very different between the 2 studies. Unfor-
a first variceal bleed5 as well as bleeding-related and tunately, both were interrupted before their recruit-
all-cause mortality,6 there has been very little study ment targets were reached. Jutabha et al.8 intended to
of its safety and efficacy in patients with high-risk enroll 104 patients but halted the study after 62 pa-
esophageal varices. The patients in this study had a tients were recruited (31 for EVL versus 31 for propran-
mean NIEC index of 37.1 with a predicted variceal olol) because of significantly increased bleeding and
bleeding rate of 50% per year. Nearly half of the pa- mortality in the propranolol group. In contrast, Norb-
tients had an NIEC index greater than 40, which has erto et al.7 interrupted a study with a similar number of
a predicted variceal bleeding rate of 63.6% per year patients because of a very low bleeding rate in both
without intervention. However, only 2 patients failed groups, which made it very unlikely that a significant
primary prophylaxis, and this resulted in a yearly difference between the groups could be demonstrated if
bleeding rate of less than 2% per year. Thus, the the planned recruitment target of 120 patients was
results of the current study show that primary pro- reached.
phylaxis with EVL produces a major reduction in the Consistent with these previous reports, the findings
expected variceal bleeding rate in patients with ad- of the current study, which is the largest reported ex-
vanced liver disease listed for liver transplantation. perience using EVL as primary prophylaxis in liver
Although 25% of the patients in our series were re- transplant candidates, show that the risk of dying from
ceiving propranolol therapy, often in very low doses, variceal bleeding while a patient is waiting for liver
there was no evidence that this conferred any addi- transplantation can be largely eliminated by a program
tional benefit in comparison with EVL alone. As such, of aggressive variceal ligation. We chose EVL as the
we routinely perform upper gastrointestinal endos- cornerstone of primary prophylaxis in this high-risk
copy on all patients with cirrhosis referred to our liver population for several reasons. The first was the con-
transplant unit, regardless of beta-blocker status, in cern that a substantial proportion of patients (between
order to screen for high-risk varices and perform pri- 30% and 50% of patients in different studies) who re-
mary prophylaxis as required. ceive apparently therapeutic doses of beta-blockers do
There have been 2 recent studies comparing the effi- not achieve a significant fall in portal pressure and
cacy and safety of EVL versus beta-blockade in high- therefore remain at high risk of bleeding.4 Furthermore,
risk patients awaiting liver transplantation.7,8 Both without monitoring the hepatic venous pressure gradi-
showed that EVL was highly effective, reducing the ent,one cannot determine whether beta-blockade has
variceal bleeding rates to zero in patients with a pre- been effective in lowering portal pressure. We felt that
dicted variceal bleeding rate of approximately 30% or this was a particular concern in liver transplantation
more after 1 year. However, the conclusions reached candidates with end-stage chronic liver disease who
regarding the efficacy of beta-blockade in this patient were at high risk of dying following variceal bleeding. In
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1512 LIM, GOW, AND ANGUS

contrast, the likely efficacy of EVL is immediately ap- rate.13 It should be noted that this meta-analysis re-
parent at the time of endoscopy, and further sessions of viewed trials that included less sick patients (eg, only
banding can be performed to ensure rapid eradication 14% of patients in Lo et al.’s study14 who underwent
of varices in those with persistent at-risk varices. A EVL had Child-Pugh C cirrhosis versus 80.2% of our
second concern was that patients with advanced liver patients, and only 9.1% of the patients in Lui et al.’s
failure are less able to tolerate beta-blockade. Indeed, in study15 had grade III/IV varices in their EVL arm ver-
the study by Norberto et al.,7 16% of patients in the sus 100% of our patients).
beta-blocker arm were forced to cease therapy because In deciding which prophylactic approach should be
of intolerance, and some were changed to banding for preferred in liver transplant candidates, we need to
prophylaxis. A significant number of patients were able weigh the major reduction in the risk of esophageal
to tolerate only what many would consider to be sub- variceal bleeding achieved with EVL against the small
therapeutic doses. Similarly in our study, of patients risk of EVL-induced ulcer bleeding and the ongoing
who were given beta-blockers, 40% were able to tolerate uncertainty regarding the relative efficacy and tolera-
only 20 mg or less of propranolol per day. bility of beta-blockade in this population. The current
The very low rate of variceal bleeding in our high-risk study shows that in this population, EVL is highly ef-
patient group supports the use of EVL as primary pro- fective in preventing first variceal bleed. Prophylactic
phylaxis in this population. In fact, bleeding rates in EVL does carry a small risk of band-induced bleeding,
our study and the previous 2 randomized studies in which is associated with significant morbidity. How-
liver transplant candidates were lower than those in ever, the rate of bleeding from band-induced ulcers is
many other studies of EVL prophylaxis. A recent meta- very low in comparison with the predicted rate of
analysis of studies comparing EVL with beta-blockade variceal bleeding.
for the primary prophylaxis of esophageal variceal hem-
orrhage reported that 10% of patients in the EVL arm
developed esophageal variceal bleeding.13 The results REFERENCES
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LIVER TRANSPLANTATION.DOI 10.1002/lt. Published on behalf of the American Association for the Study of Liver Diseases
 15276473, 2009, 11, Downloaded from https://aasldpubs.onlinelibrary.wiley.com/doi/10.1002/lt.21857 by EBMG ACCESS - GHANA, Wiley Online Library on [27/02/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
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