Open Journal of Gastroenterology, 2013, 3, 317-321 OJGas Published Online November 2013 (
Predictors of early rebleeding and mortality after acute
variceal haemorrhage in patients with cirrhosis*
Iliass Charif#, Kaoutar Saada, Ihsane Mellouki, Mounia El Yousfi, Dafr Allah Benajah,
Mohamed El Abkari, Adil Ibrahimi, Nourdin Aqodad
Department of Hepatology and Gastroenterology, Hassan II University Hospital, Faculty of Medicine and Pharmacy, Sidi Moham-
med Ben Abdellah University of Fez, Fez, Morocco
Received 25 September 2013; revised 26 October 2013; accepted 14 November 2013
Copyright © 2013 Iliass Charif et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
The upper gastrointestinal bleeding from esophageal
or gastric varices is the most dangerous complication
of portal hypertension. The purpose of this study was
to identify the predictors of early rebleeding and mor-
tality after a bleeding episode. Patients and Methods:
It was a retrospective study including 215 patients
admitted in our department of hepatology and gas-
troenterology at the Hassan II University Hospital of
Fez, from January 2001 to January 2010. Results:
The mean age of our patients was 51 years. Thirty
percent of patients had cirrhosis due to virus (B or C).
The majority of patients (79%) had only esophageal
varices. Fifty patients (23%) had a bleeding recur-
rence. Twenty-five patients (11.5%) died during the
first ten days, of which 52% had presented rebleeding
(p = 0.01). In 30% of cases, the rebleeding was secon-
dary to a fall of pressure ulcers. Univariate analysis
showed that early mortality of patients was signifi-
cantly associated with advanced age (p = 0.018), low
prothrombin time (PT) (p = 0.022), low serum sodium
(p = 0.03), low platelet count (p = 0.05), and elevated
transaminases (p = 0.02). Conclusion: The survival of
cirrhotic patients after a bleeding episode was influ-
enced by advanced age, a low rate of PT, of serum
sodium, and of the platelet count, and elevated trans-
Keywords: Cirrhosis; Portal Hypertension;
Gastrointestinal Bleeding; Esophageal Varices
The upper gastrointestinal bleeding from esophageal var-
ices is one of the most dangerous complications of portal
hypertension, with a consistently high morbidity and
mortality [1,2]. Despite advances in the management of
variceal bleeding, mortality following a bleeding epi-
sode in cirrhotic patients has decreased by only 20%
[3,4]. Several risk factors associated with mortality after
a bleeding episode were identified. These factors are:
active bleeding during the initial endoscopy, venous
pressure gradient, portal vein thrombosis, alcoholic liver
disease, bilirubin, albumin, hematocrit, transaminases,
encephalopathy, hepatocellular carcinoma and Child
Pugh score [5,6]. Many of these data were collected from
retrospective studies where mortality after variceal
bleeding was greater than 50%. But these studies have
included a relatively small number of patients, or groups
with no standard treatment especially concerning the use
of antibiotics [5,7,8]. Several prognostic scores have
been developed in cirrhotic patients with variceal bleed-
ing. Currently, the most used are the Child-Pugh score
and MELD. Recent studies have demonstrated the ability
of these scores to predict early mortality in these patients
[9]. Given the significant changes in the natural history
of cirrhosis from the broad and standardized use of anti-
biotic prophylaxis and endoscopic treatment, and given
the etiological feature of cirrhosis in our population
characterised by the high prevalence of viral cirrhosis,
we have found that it is very interesting to investigate
predictor factors of rebleeding and those involved in the
short-term survival of cirrhotic patients with variceal
2.1. Study Population
We present a retrospective study of patients with cirrho-
sis and variceal bleeding, admitted in our department of
hepatology and gastroenterology at the University Hos-
*Conflicts of interest: No conflicts of interest.
#Corresponding author.
I. Charif et al. / Open Journal of Gastroenterology 3 (2013) 317-321
pital of Fez, between January 2001 and January 2010.
We have included only patients presenting a first bleed-
ing episode. The diagnosis of cirrhosis was based on the
combination of clinical, biological, endoscopic and ultra-
sonographic criteria. The diagnosis of variceal bleeding
was confirmed by the presence of hematemesis and/or
melena at admission of our patients, and the presence of
varices at endoscopy with or without active bleeding and
without any other causes of bleeding highlighted in the
endoscopy. All patients were treated by esophageal
varices ligature associated with an antibiotic prophylaxis
based on cephalosporins, and transfusion if necessary.
During the study period, no patients had received treat-
ment with vasoactive drugs. We did not take into account
the experience of the operator who performed the hae-
mostatic action.
2.2. Variables Studied
All patients had received a biological assessment within
24 hours after the bleeding episode.
The variables studied were: age, sex, presence of as-
cites, encephalopathy, the presence of active bleeding,
lesions found at endoscopy, the platelet count, transami-
nases, prothrombin, the etiology of cirrhosis and child.
Rebleeding was defined according to the criteria of
Baveno V [10].
Early mortality was defined as death within 6 weeks
after the bleeding episode.
2.3. Statistical Methods
We conducted a descriptive analysis of data using the
Epi Info system and analytical one using the “t” Student
test. We have considered p < 0.05 as a significant value.
Between January 2001 and January 2010, 215 patients
with cirrhosis were included. The clinical characteristics
of patients are shown in Table 1. The average age was
51 years old, with an equal number of men and women.
Forty-one percent of patients had viral cirrhosis B and
18% had viral cirrhosis C, 67% of patients had Child B
and 22% had Child C. Forty-nine percent of patients had
ascites. The majority of patients (82%) had esophageal
varices alone, and 18% had esophageal varices asso-
ciated with gastric varices. Active bleeding at initial en-
doscopy was found in 66 patients (30%). The mean he-
moglobin level at admission was 8.7 g/dl, 42% of pa-
tients had received a blood transfusion during the first 24
hours of hospitalization (Table 1).
Fifty patients (23%) had rebleeding. Univariate analy-
sis showed that rebleeding was significantly associated
with the presence of a lowered prothrombin time (p =
0.05). Ascites was noted in 40% of patients with recur-
rence of bleeding (p = 0.1). The mean hemoglobin level
was 8.7 (p = 0.2), with an average number of units
transfused 2 (p = 0.1). The mean bilirubin was 16.85% (p
= 0.41). 60% of patients with recurrence had a Child B (p
= 0.2). Active bleeding at initial endoscopy was noted in
34% of cases (p = 0.3) (Table 2).
Twenty five (11.5%) patients died during the first ten
days, whose 52% had presented rebleeding (p = 0.01);
30% were secondary to an ulcer fall (p = 0.4). Univariate
analysis showed also that early mortality of patients was
significantly associated with advanced patients age (p =
0.018), low prothrombin time (p = 0.022), low serum
sodium (p = 0.03), low platelet count (p = 0.05), and
elevated transaminases (p = 0.02) (Table 3).
The rate of rebleeding in our study was 23% , this rate is
lower than that reported by Wang M et al. [11] in 2011
(35.8%) and Ben-Ari Z et al. [12] in 1999 (44%), but
approximately equal to that reported in the study of Krig
JE et al. [13] in 2009 (24%). This difference could be
due to a difference in treatment methods. Ben-Ari Z and
colleagues [12] treated their patients by blood transfu-
Table 1. Clinical and biological characteristics of the study
population (N = 215).
Number of patients 215
Male 107 (50%)
Mean age 51 ans
24 (11%)
145 (67%)
48 (22%)
Cause of bleeding
Esophageal varices
Gastric varices + esophageal varices
215 (82%)
37 (18%)
Clinical caracteristics of bleeding
Hématemesis + melena
Etiology of cirrhosis
Virus B
Virus C
89 (41%)
38 (18%)
88 (41%)
Mean Hemoglobin (g/dl) 8.7
Natremia (meq/l) 135.7
Ascites 105
Transfusion in the first 24 hours 92 (24%)
Average number of units transfused 1.17
Varices with red signs 149
Varices with actif bleeding 66 (30%)
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I. Charif et al. / Open Journal of Gastroenterology 3 (2013) 317-321 319
Table 2. Predictors of rebleeding: univariate analysis.
No rebleeding:
N = 165
N = 50 p
Mean age (an) 51 ans 50 ans 0.7
Male (%) 50% 50% 0.5
Ascites 85 (51%) 20 (40%) 0.1
Hepatic encephalopathy 11 (6%) 3 (6%) 0.5
Active bleeding 49 (29.7%) 17 (34%) 0.6
Esophageal varices
grade III 68 (41%) 18 (36%) 0.5
Gastric varices 27 (16%) 10 (20%) 0.5
Platelets 107,805 109,608 0.8
Transférase (GPT) 48 68 0.2
Prothrombin time 70% 59% 0.05
Child A
Child B
Child C
17 (10%)
107 (64%)
43 (26%)
6 (12%)
34 (68%)
6 (12%)
Table 3. Predictors of early mortality: univariate analysis.
Patients survived
N = 190
Patients died
N = 25 (11.6%) p
Age (an) 50.53 58.84 0.018
Male (%) 51% 40% 0.3
Ascites 91 (48%) 14 (56%) 0.5
encephalopathy 10 (5.2%) 4 (16%) -
Rebleeding 37 (19.5%) 13 (52%) 0.01
Platelets 132,590 105,053 0.05
Prothrombin time 69% 57% 0.02
Transférase (GPT) 44.6 114 0.02
Serum albumin 30 25 0.19
Serum creatinine 9.68 11.39 0.45
Natremia 136 132 0.03
Child A
Child B
Child C
245 (13.2%)
126 (96.6%)
31 (17%)
2 (14.2%)
6 (42.8%)
6 (42.8%)
sions and vasoactive drugs, and if failure, sclerosis of
esophageal varices was performed. In the study of Wang
M et al. [11], patients were also treated with blood trans-
fusions, vaso active drugs and anti acids. However, Krige
JE and colleagues [13] treated their patients by sclerosis
of esophageal varices. In our study, all patients were
treated by endoscopic band ligation. The comparison
between these series allows us to conclude that endo-
scopic therapy may be effective in cirrhotic patients with
bleeding esophageal varices, this should be confirmed by
other studies. In the study by Wong et al. [11], univariate
analysis revealed that a low albumin levels, high white
blood cell count, score of Child B and C, the presence of
ascites, and encephalopathy were predictors of rebleed-
ing in cirrhotic patients, these results were similar to
those found in several studies [14-18]. In our study, these
factors were not significantly associated with rebleeding,
and only a low rate of prothrombin was a predictor of
recurrence. This result implies that the severity of co-
agulopathy may play a critical role in rebleeding. In the
series of K Bambha et al. [19], the MELD score and the
presence of platelet plug on varicose veins in the initial
endoscopy were predictive of rebleeding. Stratification
of patients according to the MELD score (MELD 18
points, MELD < 18 points) revealed a significant in-
crease in the risk of rebleeding in patients with a MELD
score 18 points. Currently, there is no well-established
model to accurately predict the survival of cirrhotic pa-
tients after an episode of gastrointestinal bleeding due to
rupture of esophageal varices. One of the difficulties is
that the prognosis for these patients is influenced not
only by the severity of the bleeding episode itself, but
also by the severity of the underlying liver disease. In our
series, the advanced age of patients was predictive of
mortality in the first six weeks after the bleeding episode,
this was consistent with the series of Sempere L et al.
[20] who found that age 65 years was significantly
associated with early mortality. This factor is probably
related to some factors found in the elderly population,
mainly the duration of progression of liver disease, and
the greater difficulty of management of recurrent de-
compensation [21]. In this series, the presence of HCC,
the incidence of infection during the bleeding episode, a
Child score 10 and MELD score 18 were also asso-
ciated with early mortality. Some authors suggest that the
development of HCC may accelerate the course of liver
disease [22]. These patients often have a portal vein
thrombosis, rebleeding after endoscopic treatment and
thus a higher risk of early mortality. This high mortality
rate is probably secondary to the advanced state of the
underlying cirrhosis and the difficulty of mastering portal
hypertension resulting [23-25]. In the series of Bamba K
et al, advanced Child score, MELD score 18, the
number of units transfused during the first 24 hours, the
presence of ascites, an active bleeding at initial endo-
scopy, high transaminase levels and low serum sodium
were predictive of early mortality. The last two parame-
ters were also found in our study, which was consistent
with other studies [26]. The occurrence of rebleeding
during the first five days after the bleeding was signifi-
cantly associated with early mortality in our series, a
Copyright © 2013 SciRes. OPEN ACCESS
I. Charif et al. / Open Journal of Gastroenterology 3 (2013) 317-321
factor also reported in the series of Kamba et al. [19].
The degree of liver cell failure influenced the occurrence
of rebleeding after an episode of variceal bleeding in
cirrhotic patients. The advanced age of patients, low
prothrombin time, low rates of serum sodium and of
platelets count, and high transaminase rate were predic-
tors of early mortality in these patients.
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