s43066 020 00027 X
s43066 020 00027 X
s43066 020 00027 X
Abstract
Background: Development of esophageal varices (EVs) is the main complication of portal hypertension. Early detection
prevents variceal bleeding. Baveno VI consensus recommended endoscopy if transient elastography (TE) > 20 kPa and
platelets below 150,000/mm3.
Aim: Assessment of the reliability of the albumin-bilirubin (ALBI), platelets-albumin-bilirubin (PALBI), albumin-bilirubin-platelets
(ALBI-PLT) score, and gamma-glutamyl transferase-platelets (GAR) ratio as non-invasive models for prediction of EVs presence
and the need for endoscopy in patients with HCV-related cirrhosis.
Methods: HCV-related F4 fibrosis by TE or cirrhosis patients were included (n = 661). Full metabolic profile, CBC,
ultrasonography, and endoscopy were done.
Results: The average age was 42.89 years mainly males. Patients with EVs had statistically significant (p < 0.05) higher TE
values, ALBI, ALBI-PLT, and PALBI than those without EVs. Both groups were comparable for GAR. Large varices were
statistically (p < 0.05) associated with higher ALBI, ALBI-PLT, and PALBI. Both small and large varices had comparable TE and
GAR. EVs detection cutoffs (sensitivity, specificity): TE > 20 kPa (83.64%, 91.62%), ALBI >− 2.43 (81.28%, 74.89%), ALBI-PLT > 3
(77.34%, 72.93%), and PALBI >− 2.28 (62.1%, 76.4%). On comparison of the ROCs, TE was better than ALBI (p < 0.05), ALBI-PLT,
and PALBI. ALBI was better than ALBI-PLT and PALBI. Both ALBI-PLT and PALBI are comparable (p > 0.05). Positive indirect
hemagglutination of schistosomiasis, portal vein diameter, splenic vein diameter, TE, ALBI, ALBI-PLT, and PALBI were
independent predictors of EVs existence. On multivariate analysis, portal vein diameter, TE, and ALBI score were significant.
Conclusion: The ALBI, ALBI-PLT, and PALBI are useful predictors of EVs presence and the need of diagnostic endoscopy
especially in centers that lack FibroScan.
Keywords: HCV, Esophageal varices, Cirrhosis, Transient elastography, ALBI, PALBI, ALBI-PLT
© The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License,
which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give
appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if
changes were made. The images or other third party material in this article are included in the article's Creative Commons
licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons
licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain
permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
Alsebaey et al. Egyptian Liver Journal (2020) 10:22 Page 2 of 8
of the smooth muscles of the blood vessels, hepatic stellate [7, 8] or clinically diagnosed as having cirrhosis. The
cells around the sinusoids, and the myofibroblasts in the diagnosis of liver cirrhosis was done depending on the
fibrous septae, in response to increased vasoconstrictors, clinical, laboratory and radiological features by abdom-
e.g., endothelins, norepinephrine, angiotensin II, cysteinyl inal ultrasonography [9].
leukotrienes and decreased intrahepatic vasodilators as ni- Exclusion criteria included the following: dual or other
trous oxide. Splanchnic vasodilation in response to gluca- liver disease (HBV, alcohol, etc.); portal vein thrombosis;
gon, nitrous oxide, prostacyclin, bacterial translocation, gastric varices on endoscopy; history of previous endos-
and carbon monoxide is a major cause of increased portal copy; previous variceal bleeding, ascites; hepatic enceph-
venous flow [1, 3]. alopathy; and hepatocellular carcinoma.
Esophageal varices (EVs), a major complication of por- Thorough history taking and complete clinical exam-
tal hypertension, may rupture and bleed with increased ination of the patients were done. Full metabolic profile,
mortality rate. EVs are dilated tortuous submucosal CBC, and INR were done. Gamma-glutamyl transferase
veins usually in the distal esophagus. They develop when was done only in 148 cases. All investigations were done
HVPG > 10 mmHg but bleed when HVPG > 12 mmHg within 1 week before endoscopy.
[1]. Endoscopy is the gold standard for the detection and Upper esophageo-gastroscopy was done by the same
diagnosis for the follow-up of EVs. endoscopist (A) to screen for EVs presence and grade
By doing endoscopy, we can classify variceal size, de- discrimination. EVs were classified into small and large
tect gastric varices and portal hypertensive gastropathy. varices [10].
Moreover, endoscopy is a therapeutic tool that allows Calculations:
variceal eradication, for example, band ligation and glue ALBI = (log10 bilirubin μmol/L × 0.66) + (albumin g/L ×
obturation of gastric varices [4]. − 0.085) [11].
Endoscopy is costly, bothersome for the patients espe- ALBI grades: ALBI I ≤ − 2.60, ALBI II > − 2.60 to ≤ −
cially if done without conscious sedation. So, non- 1.39 and ALBI III > − 1.39.
invasive methods for variceal detection are warranted. PALBI = (2.02 × log10 bilirubin) + (−0.37 × [log10 biliru-
Clinically, splenomegaly, platelet count, and platelet to bin]2) + (−0.04 × albumin) + (−3.48 × log10 platelets) +
spleen ratio > 909 are suggestive of portal hypertension. (1.01 × [log10 platelets]2) [12, 13].
Radiologically, Doppler, CT, and MRI can detect varices. PALBI grades: PALBI grade 1: value ≤ − 2.53, PALBI
Furthermore, liver stiffness measured by transient elasto- grade 2: value from − 2.53 to − 2.09, PALBI grade 3:
graphy (TE) as with FibroScan can predict EVs. Recently, value > − 2.09
endoscopic video capsule can diagnose EVs but cannot ALBI-PLT = sum of the ALBI grade (I–III) to the plate-
assess the size [5]. let count grade (I–II). Grade I platelet count = platelets >
On the one hand, the Baveno VI consensus [6] recom- 150,000/mm3 and grade II platelet count = platelets ≤ 150,
mended screening endoscopy in patients with liver transi- 000/mm3. The ALBI PLT range is 2–5 [14].
ent elastography (TE) > 20 kPa and platelets < 150,000/ GAR = gamma − glutamyl transferase (U/L)/plate-
mm3 and vice versa. On the other hand, the TE measure- lets mm3 × 100 [15].
ment by FibroScan is not available in all hospitals. N.B. GAR was calculated for 77 patients without vari-
In clinical practice, the physician needs models based on ces, 71 patients with EVs (24 small varices and 47 large
the routine investigations to alarm him about the prob- varices).
ability of esophageal varices and need of the endoscopy.
This study aimed at assessing albumin-bilirubin (ALBI), Statistical analysis
platelets-albumin-bilirubin score (PALBI), albumin-bilirubin- Data were statistically analyzed using IBM® SPSS® Statis-
platelets grade (ALBI-PLT), and gamma-glutamyl transferase- tics® version 21 for Windows (IBM Corporation, North
platelets (GAR) ratio as non-invasive models for prediction of Castle Drive, Armonk, NY, USA) and MedCalc® version
EVs presence and the need for endoscopy in patients with 18.2.1 (Seoul, Republic of Korea). Data were expressed
HCV-related cirrhosis. as mean ± standard deviation, median (interquartile
range) for data that are not normally distributed and col-
Methods umn percentage for nominal data. All p values are 2
This study was conducted in the National Liver Institute tailed, with values < 0.05 considered statistically signifi-
hospitals, Menoufia University. After patient education cant, p = 0.01 is highly significant and p = 0.001 is very
and answering for all questions, an informed consent highly significant. Comparisons between two groups
was signed by all patients. The study was approved by were performed using Student’s t test for parametric
the institutional review board. data, and Mann-Whitney test for non-parametric data.
Six hundred sixty-one HCV patients with F4 fibrosis Chi-squared test (χ2) and Fisher exact test for categorical
as measured by transient elastography (n = 423, 62.5%) data analysis. The receiver operating characteristic
Alsebaey et al. Egyptian Liver Journal (2020) 10:22 Page 3 of 8
Table 1 Baseline characteristics, investigations, and scores (ROC) curve analysis was used for detection of the cut-
No EVs EVs p off value for the esophageal varices presence and for
N = 458 N = 203 small versus large varices size discrimination. For each
Age (years) 40.48 ± 11.38 51.16 ± 8.55 0.001# cutoff, sensitivity, specificity, positive predictive value,
40 (17) 51 (9)
and negative predictive value were calculated. The ROCs
Sex Female 131 (28.6%) 65 (32.0%) 0.406 were compared using the DeLong tests to assess variable
Male 327 (71.4%) 138 (68.0%) discrimination. Univariate and multivariate binary logis-
IHA Sch. Negative 320 (89.4%) 43 (78.2%) 0.025 tic regression were done for detecting the predictors of
Positive 38 (10.6%) 12 (21.8%) esophageal varices presence irrespective of the size.
Total bilirubin (mg/dL) 1.26 ± 1.74 2.01 ± 2.16 0.001#
0.85 (0.5) 1.5 (1.4) Results
Albumin (mg/dL) 3.96 ± 0.82 3.09 ± 0.81 0.001# Table 1 demonstrates comparison between patients with
4.2 (0.8) 3.1 (1.1)
and without esophageal varices. Patients with esophageal
AST (U/L) 55.43 ± 41.26 78.40 ± 115.99 0.001#
45 (34) 59 (47) varices compared to those without varices, were older
ALT (U/L) 55.59 ± 48.14 57.41 ± 75.28 0.912#
(51.16 ± 8.55 vs. 40.48 ± 11.38 years; p = 0.001) and
45 (34) 46 (39) positive for indirect hemagglutination of schistosomiasis
GGT (U/L) 64.47 87.14 63.70 ± 69.60 0.338# (21.8% vs. 10.6%; p = 0.025).
32 (56.5) 34 (52) Patients with esophageal varices had statistically sig-
Hemoglobin (g/dL) 13.48 ± 1.51 12.25 ± 3.06 0.001# nificant (p < 0.05) higher value [median (IQR)] of serum
13.5 (2.1) 12 (2.8)
total bilirubin [1.5 (1.4) vs. 0.85 (0.5) mg/dL], serum
WBCs (/mm3) 6.52 ± 7.16 4.60 ± 1.44 0.001#
5.9 (3) 4.45 (2) AST [59 (47) vs. 45 (34) U/L], INR [1.3 (0.2) vs. 1.1
Platelets (109/L) 175.99 ± 66.72 92.42 ± 39.39 0.001
(0.2)], liver stiffness [29.6 (16.7) vs. 16.8 (7.9) kPa], portal
175 (90) 89 (54) vein diameter [13 (2) vs. 11 (2) cm], and splenic vein
Platelets (/mm3) ≥ 150109/L 308 (96%) 13 (4%) 0.001 diameter.
< 150109/L 150 (44.1%) 190 (55.9%) Meanwhile, they had statistically significant (p < 0.05)
INR 1.17 ± 0.28 1.33 ± 0.28 0.001# lower value [median (IQR)] of serum albumin [3.1 (1.1)
1.1 (0.2) 1.3 (0.2) vs. 4.2 (0.8) mg/dL], hemoglobin [12 (2.8) vs. 13.5 (2.1)
Portal vein diameter (cm) 11.39 ± 1.53 13.17 ± 2.36 0.001# g/dL], WBCs [4.45 (2) vs. 5.9 (3) mm3] and platelets [89
11 (2) 13 (2)
(54) vs. 175 (90) 109/L]. About 55.9% of the patients
Splenic vein diameter (cm) 9.28 ± 1.09 9.60 ± 1.51 0.052# with EVs had platelets < 150,000 mm3.
9 (1) 9 (1)
Patients with esophageal varices compared to those
Transient elastography (kPa) 17.54 ± 6.46 31.92 ± 13.29 0.001#
16.8 (7.9) 29.6 (16.7) without varices (Table 1 and Fig. 1) had statistically sig-
ALBI score − 2.58 ± 0.84 − 1.71 ± 0.81 0.001# nificant (p < 0.05) higher value [median (IQR)] of ALBI
− 2.84 (0.7) − 1.68 (1.16) score [− 1.68(1.16) vs. − 2.84(0.7)], ALBI-PLT score
ALBI grade 1 310 (67.7%) 31 (15.3%) 0.001 [4(1) vs. 2(2)], and PALBI score ( 2.09 ± 0.55 vs. − 2.46
2 91 (19.9%) 106 (52.2%) ± 0.51). Both groups were comparable as regards GAR
3 57 (12.4%) 66 (32.5%) (p = 0.197).
ALBI-PLT score 2.83 ± 1.04 3.99 ± 0.88 0.001# Table 2 shows discrimination of small and large vari-
2 (2) 4 (1) ces. Large varices were statistically (p < 0.05) associated
ALBI-PLT grade 2 249 (54.4%) 17 (8.4%) 0.001 with higher [median (IQR)] liver stiffness [29.8 (14.7) vs.
3 85 (18.6%) 29 (14.3%) 29 (17.1) kPa], ALBI score [− 1.47 (0.7) vs. − 2.08 (1.1)],
4 78 (17%) 96 (47.3%) ALBI-PLT score [4 (1) vs. 4 (0.5)] and PALBI score [−
5 46 (10%) 61 (30%) 1.9 (0.5) vs. − 2.34 (0.7)]. Both small and large varices
PALBI score − 2.46 ± 0.51 − 2.09 ± 0.55 0.001
had comparable GAR (p = 0.535).
The ROC curve analysis was used to assess the useful-
PALBI grade 1 252 (55%) 46 (22.7%) 0.001
ness of ALBI score, ALBI-PLT score, PALBI score, and
2 128 (27.9%) 55 (27.1%)
GAR as non-invasive models for detection of esophageal
3 78 (17%) 102 (50.2%)
varices and discrimination of its grade or size (Table 3).
GAR 1.82 ± 5.03 1.57 ± 1.61 0.197#
0.83 (1.28) 0.99 (1.2)
For variceal detection whatever the size (Figs. 2 and 4);
EVs esophageal varices, IHA Sch indirect hemagglutination of schistosomiasis
ALBI >− 2.43 had 81.28% sensitivity, 74.89% specificity,
#
Mann-Whitney test. Data are represented as mean ± standard deviation, 58.9% PPV, and 90% NPV. The ALBI-PLT score > 3 had
number (percentage) for nominal data and median (interquartile range) for 77.34% sensitivity, 72.93% specificity, 55.86% PPV, and
data out of normal distribution
87.90% NPV. The PALBI score >− 2.28 had 62.1% sensi-
tivity, 76.4% specificity, 53.8% PPV, and 82% NPV. In
Alsebaey et al. Egyptian Liver Journal (2020) 10:22 Page 4 of 8
the current study, the cut-off of the liver stiffness AUC 0.744 0.582 0.754 0.561 0.545
adopted by the Baveno VI (>− 20 kPa) had had 83.64% P 0.001 0.036 0.001 0.441 0.5431
sensitivity, 91.62% specificity, 60.5% PPV, and 97.3% 95% CI 0.678– 0.511– 0.688– 0.421– 0.422–
NPV. 0.803 0.651 0.811 0.695 0.663
Pairwise comparison of ROC curves for esophageal Cut-off >− 1.88 >4 >− 2.12
varices detection whatever the size revealed TE was bet- Sensitivity 92.96 39.44 87.32
ter than ALBI (p < 0.05), ALBI-PLT, (p < 0.05), and Specificity 60.61 75 64.39
PALBI (p < 0.05). ALBI was better than ALBI-PLT (p <
PPV 55.9 45.9 56.9
0.05) and PALBI (p < 0.05). Both ALBI-PLT and PALBI
NPV 94.1 69.7 90.4
are comparable (p > 0.05).
TE transient elastography, PPV positive predictive value, NPV negative
For large varices discrimination (Figs. 3 and 4); ALBI predictive value
>− 1.88 had 92.96% sensitivity, 60.61% specificity, 55.9%
PPV, and 94.1% NPV. The ALBI-PLT score > 4 had Pairwise comparison of ROC curves for discrimination
39.44% sensitivity, 75% specificity, 45.9% PPV, and 69.7% of large varices revealed both the ALBI score and PALBI
NPV. The PALBI score >− 2.12 had 87.32% sensitivity, score were comparable (p = 0.526). Both ALBI score and
64.39% specificity, 56.9% PPV, and 90.4% NPV. PALBI score were better than ALBI-PLT score; (p =
0.001) and (p = 0.001), respectively.
By univariate logistic regression, the following vari-
ables were statistically independent predictors for
Table 2 Comparison of TE, ALBI, ALBI-PLT, and PALBI in patients
with small and large esophageal varices
esophageal varices presence (Table 4); positive indirect
hemagglutination of schistosomiasis (odd = 2.35, 95% CI
Esophageal varices p
= 1.14–4.84), portal vein diameter (odd = 1.71, 95% CI =
Small Large
1.52–1.92), splenic vein diameter (odd = 1.24, 95% CI =
N = 132 N = 71 1.05–1.45), TE (odds = 1.25, 95% CI = 1.19–1.32), ALBI
Transient elastography (kPa) 30.84 ± 12.68 33.33 ± 14.18 0.44# score (odd = 2.94, 95% CI = 2.40–3.62), ALBI-PLT score
29(17.1) 29.8 (14.7)
(odd = 2.78, 95% CI = 2.32–3.34), and PALBI score (odd
ALBI score − 1.92 ± 0.83 − 1.29 ± 0.57 0.001# = 3.45, 95% CI = 2.50–4.76).
− 2.08(1.1) − 1.47(0.7)
On multivariate analysis, portal vein diameter, TE, and
ALBI-PLT score 3.89 ± 0.92 4.18 ± 0.78 0.039#
4(0.5) 4(1)
ALBI score were statistically independent predictors for
esophageal varices presence.
PALBI score − 2.24 ± 0.55 − 1.80 ± 0.43 0.001#
− 2.34 (0.7) − 1.9 (0.5)
Discussion
GAR 1.63 ± 1.64 1.54 ± 1.61 0.535#
1.08(1.37) 0.86(1.02) PHTN and subsequently EVs varices are the main com-
#
Mann-Whitney test. Data are represented as mean ± standard deviation and
plications of liver cirrhosis. Once the EVs bleed, the hep-
median (interquartile range) for data out of normal distribution atic reserve begins to decrease with each attack since the
Alsebaey et al. Egyptian Liver Journal (2020) 10:22 Page 5 of 8
Fig. 4 the cutoffs pf ALBI, ALBI-PLT and PALBI for esophageal varices and large varices discrimination
three score were the same statistically for the 1 year PPV, and 97% NPV for detecting HRVs. It is very simple
mortality. score that also incorporated the dysfunction grade and
Zou et al. [28] found that ALBI score >− 1.492 had PHTN indirectly. ABLI-PLT could discriminate patients
100% sensitivity, 69.62% specificity, 7.4% PPV, and 100% with HRVs so it is a simple non-invasive screening tool
NPV for predicting acute upper gastrointestinal and obviated unnecessary endoscopy.
hemorrhage-related in-hospital mortality of in liver cir- In the current study, patients with EVs had more inci-
rhosis. The etiology of cirrhosis was, HBV, HCV, alco- dence of Schistosomiasis 21.8% against 10.6%. Schisto-
hol, or mixed. Unfortunately, the AUC of ALBI score somiasis per se is a major cause of presinusoidal PHTN
was statistically comparable to the CTP and MELD but it may augment the effect of HCV on the liver sub-
score, so it did not add benefit [28]. sequently PHTN [29, 30]. The increased serum bilirubin,
Recently, Chen et al. [14] developed new score (ALBI- portal vein diameter and the decreased level of serum al-
PLT) to screen for high-risk esophageal varices (HRVs) bumin, hemoglobin, WBCs and platelets reflect liver
in patients with HCC. He combined the ALBI grade (I– dysfunction, PHTN, and splenic sequestration or hypers-
III) to platelets grade (I–II) so the sum ranged from 2 to plenism in patients with EVs.
5. HRVs were common with ALBI grade II > I. ALBI- In fact ALBI, PALBI, and ALBI-PT scores could reflect
PLT score > 2 had 90% sensitivity, 27% specificity, 21% the degree of liver dysfunction and PHTN since higher
values were seen in patients with EVs. Furthermore, they (90% vs. 77.34%) and very low specificity (27% vs.
were of higher values in patients with large varices com- 72.93%).
pared to small varices. The limitations of the study are that it is single-center
Despite the promising studies of GAR value in patients experience, did not assess the longitudinal follow-up
with HBV-related fibrosis [15, 20, 31], some studies did mortality, and did not assess them in non-HCV liver dis-
not find this advantage compared to other score in pa- eases or patients with ascites nor HCC. Large number
tients with HBV fibrosis [32, 33]. Shimakawa et al. [34] multi-centric studies are needed.
conducted the first study of GAR in patients with HCV
fibrosis. GAR was comparable to APRI and Fib-4 score. Conclusion
In our study, it was useless for the diagnosis and dis- The ALBI, ALBI-PLT, and PALBI are useful predictors
crimination of EVs though the number of patient with of EVs presence and the need of diagnostic endoscopy
data was relatively low. especially in centers that lack FibroScan.
For EVs prediction, ALBI >− 2.43 had 81.28% sensitiv-
Abbreviations
ity and 74.89% specificity. The ALBI-PLT score > 3 had PHTN: Portal hypertension; HVPG: Hepatic venous pressure
77.34% sensitivity and 72.93% specificity. The PALBI gradientEVsEsophageal varices; ALBI: Albumin-bilirubin; PALBI: Platelets-
score >− 2.28 had 62.1% sensitivity and 76.4% specificity. albumin-bilirubin; ALBI-PLT: Albumin-bilirubin-platelets; GAR: γ-Glutamyl
transferase-platelets; IHA Sch: Indirect hemagglutination; AUC: Area under
ALBI >− 1.88 (92.96% sensitivity, 60.61% specificity), the curve; CTP: Child-Pugh; HRVs: High risk esophageal varices; PPV: Positive
ALBI-PLT score > 4 (39.44% sensitivity, 75% specificity), predictive value; NPV: Negative predictive value; CI: Confidence interval;
and PALBI score >− 2.12 (87.32% sensitivity, 64.39% TE: Transient elastography
specificity) could discriminate large from small varices.
Acknowledgements
Again which one is the best? The ALBI-PLT score was None
less effective than ALBI and PALBI for EVs size
discrimination. Authors’ contributions
Data collection: AA, HMA, MAE. Study design: AA, HMA, MAE. Manuscript
The ROC analysis of the TE cutoff (> 20kPa) adopted by writing and final revision: AA. All authors have read and approved the
the Baveno VI consensus [6] in our study showed 83.64% manuscript
sensitivity and 91.62% specificity. Thrombocytopenia
Funding
< 150,000/mm3 was statistically associated with EVs but None
the percentage is not too high (55.9%).
On comparison of the different ROCs liver stiffness Availability of data and materials
measured by FibroScan was better than all other scores, The datasets used and/or analyzed during the current study are available
from the corresponding author on reasonable request.
namely, ALBI, ALBI-PLT, and PALBI. In fact, ALBI was
better than ALBI-PLT and PALBI. Both ALBI-PLT and Ethics approval and consent to participate
PALBI were comparable. It is approved by National Liver Institute IRB 0085/2014. Informed written
consent was signed by all patients.
Regarding the size of the varix, TE did not add benefit
unlike the other scores where the ALBI and PALBI were Consent for publication
the best for variceal size discrimination. Not applicable
Positive indirect hemagglutination of schistosomiasis,
Competing interests
portal vein diameter, splenic vein diameter, liver stiff- None
ness, ALBI score, ALBI-PLT score, and PALBI score
Received: 13 October 2019 Accepted: 19 March 2020
were independent predictors of EVs existence. On multi-
variate analysis, portal vein diameter, TE, and ALBI
score were statistically independent predictors for References
esophageal varices presence. 1. Shung DL, Garcia-Tsao G (2017) Liver Capsule: Portal hypertension and
varices: pathogenesis, stages, and management. Hepatology 65:1038
As aforementioned, three studies were conducted on 2. Treiber G, Csepregi A, Malfertheiner P (2005) The pathophysiology of portal
relationship of ALBI and ALBI-PLT and portal hyper- hypertension. Digest Dis 23:6–10
tension reflected by variceal bleeding [27, 28] or the 3. Iwakiri Y (2014) Pathophysiology of portal hypertension. Clin Liver Dis 18:
281–291
presence of HRVs [14]. None of them assessed the 4. Gulamhusein AF, Kamath PS (2017) The epidemiology and pathogenesis of
PALBI score. We are the first study to assess PALBI gastrointestinal varices. Tech Gastrointest Endo 19:62–68
score and the role of the three scores in screening for 5. de Franchis R, Dell’Era A (2014) Invasive and noninvasive methods to
diagnose portal hypertension and esophageal varices. Clin Liver Dis 18:293–
EVs in cirrhosis patients without hepatocellular 302
carcinoma. 6. de Franchis R (2015) Expanding consensus in portal hypertension: report of
The cutoff of ALBI-PLT was lower than our study (2 the Baveno VI Consensus Workshop: Stratifying risk and individualizing care
for portal hypertension. J Hepatol 63:743–752
vs. 4–5) [14]. The possible explanations that the authors 7. Arena U, Lupsor Platon M, Stasi C, Moscarella S, Assarat A, Bedogni G et al
compared to us chose a cutoff value with high sensitivity (2013) Liver stiffness is influenced by a standardized meal in patients with
Alsebaey et al. Egyptian Liver Journal (2020) 10:22 Page 8 of 8
chronic hepatitis C virus at different stages of fibrotic evolution. Hepatology 28. Zou D, Qi X, Zhu C, Ning Z, Hou F, Zhao J et al (2016) Albumin-bilirubin score
58:65–72 for predicting the in-hospital mortality of acute upper gastrointestinal bleeding
8. de Ledinghen V, Vergniol J (2010) Transient elastography for the diagnosis of in liver cirrhosis: a retrospective study. Turk J Gastroenterol 27:180–186
liver fibrosis. Expert Rev Med Devices 7:811–823 29. Chofle AA, Jaka H, Koy M, Smart LR, Kabangila R, Ewings FM et al (2014)
9. Tsochatzis EA, Bosch J, Burroughs AK (2014) Liver cirrhosis. Lancet 383:1749– Oesophageal varices, schistosomiasis, and mortality among patients
1761 admitted with haematemesis in Mwanza, Tanzania: a prospective cohort
10. Lee UE, Friedman SL (2011) Mechanisms of hepatic fibrogenesis. Best Pract study. BMC Infect Dis 14:303
Res Clin Gastroenterol 25:195–206 30. Bahgat MM (2014) Interaction between the neglected tropical disease
11. Johnson PJ, Berhane S, Kagebayashi C, Satomura S, Teng M, Reeves HL et al human schistosomiasis and HCV infection in Egypt: a puzzling relationship.
(2015) Assessment of liver function in patients with hepatocellular carcinoma: Journal of Clinical and Translational Hepatology 2:134–139
a new evidence-based approach—The ALBI Grade. J Clin Oncol 33:550–558 31. Ren T, Wang H, Wu R, Niu J (2017) Gamma-glutamyl transpeptidase-to-
12. Elshaarawy O, Allam N, Abdelsameea E, Gomaa A, Waked I (2020) Platelet- platelet ratio predicts significant liver fibrosis of chronic hepatitis B patients
albumin-bilirubin score - a predictor of outcome of acute variceal bleeding in China. 2017:7089702
in patients with cirrhosis. World J Hepatol 12(3):99–107 32. Li Q, Song J, Huang Y, Li X, Zhuo Q, Li W et al (2016) The gamma-glutamyl-
13. Elshaarawy O, Alkhatib A, Elhelbawy M, Gomaa A, Allam N, Alsebaey A et al transpeptidase to platelet ratio does not show advantages than APRI and
(2019) Validation of modified albumin-bilirubin-TNM score as a prognostic Fib-4 in diagnosing significant fibrosis and cirrhosis in patients with chronic
model to evaluate patients with hepatocellular carcinoma. World J Hepatol hepatitis B: a retrospective cohort study in China. Medicine 95:e3372
11:542–552 33. Huang R, Wang G, Tian C, Liu Y, Jia B, Wang J et al (2017) Gamma-glutamyl-
14. Chen P-H, Hsieh W-Y, Su C-W, Hou M-C, Wang Y-P, Hsin IF et al (2018) transpeptidase to platelet ratio is not superior to APRI,FIB-4 and RPR for
Combination of albumin-bilirubin grade and platelet to predict diagnosing liver fibrosis in CHB patients in China. Sci Rep 7:8543
compensated patient with hepatocellular carcinoma who do not require 34. Shimakawa Y, Bonnard P, El Kassas M, Abdel-Hamid M, Esmat G, Fontanet A
endoscopic screening for esophageal varices. Gastrointestinal Endos (2016) Diagnostic accuracy of the γ-glutamyl transpeptidase to platelet ratio
15. Lemoine M, Shimakawa Y, Nayagam S, Khalil M, Suso P, Lloyd J et al (2016) to predict liver fibrosis in Egyptian patients with HCV genotype 4. Gut 65:
The gamma-glutamyl transpeptidase to platelet ratio (GPR) predicts 1577–1578
significant liver fibrosis and cirrhosis in patients with chronic HBV infection
in West Africa. Gut 65:1369–1376 Publisher’s Note
16. Kao W-Y, Su C-W, Chiou Y-Y, Chiu N-C, Liu C-A, Fang K-C et al (2017) Springer Nature remains neutral with regard to jurisdictional claims in
Hepatocellular carcinoma: nomograms based on the albumin-bilirubin published maps and institutional affiliations.
grade to assess the outcomes of radiofrequency ablation. Radiology 285:
670–680
17. Hiraoka A, Kumada T, Kudo M, Hirooka M, Tsuji K, Itobayashi E et al (2017)
Albumin-bilirubin (ALBI) grade as part of the evidence-based clinical
practice guideline for HCC of the Japan Society of Hepatology: a
comparison with the liver damage and Child-Pugh classifications. Liver
Cancer 6:204–215
18. Hiraoka A, Michitaka K, Kumada T, Kudo M (2017) ALBI score as a novel tool
in staging and treatment planning for hepatocellular carcinoma: advantage
of ALBI grade for universal assessment of hepatic function. Liver Cancer 6:
377–379
19. Hansmann J, Evers MJ, Bui JT, Lokken RP, Lipnik AJ, Gaba RC et al (2017)
Albumin-bilirubin and platelet-albumin-bilirubin grades accurately predict
overall survival in high-risk patients undergoing conventional transarterial
chemoembolization for hepatocellular carcinoma. J Vasc Interv Radiol 28:
1224–31.e2
20. Liu PH, Hsu CY, Hsia CY, Lee YH, Chiou YY, Huang YH et al (2017) ALBI and
PALBI grade predict survival for HCC across treatment modalities and BCLC
stages in the MELD Era. J Gastroenterol Hepatol 32:879–886
21. Chen RC, Cai YJ, Wu JM, Wang XD, Song M, Wang YQ et al (2017)
Usefulness of albumin-bilirubin grade for evaluation of long-term prognosis
for hepatitis B-related cirrhosis. J Viral Hepatitis 24:238–245
22. Shao L, Han B, An S, Ma J, Guo X, Romeiro FG et al (2017) Albumin-to-
bilirubin score for assessing the in-hospital death in cirrhosis. Translat
Gastroenterol Hepatol 2:88
23. Chen B, Lin S (2017) Albumin-bilirubin (ALBI) score at admission predicts
possible outcomes in patients with acute-on-chronic liver failure. Medicine
96:e7142
24. Hou YL, Gao MD, Guo HY, Wang R, Wang Z, Yu YH et al (2018) Diagnostic
value of albumin-bilirubin grade combined with serum ammonia in
cirrhosis with hepatic encephalopathy. Zhonghua yi xue za zhi 98:127–131
25. Chan AW, Chan RC, Wong GL, Wong VW, Choi PC, Chan HL et al (2015)
New simple prognostic score for primary biliary cirrhosis: Albumin-bilirubin
score. J Gastroenterol Hepatol 30:1391–1396
26. Ronald J, Wang Q, Choi SS, Suhocki PV, Hall MD, Smith TP et al (2017)
Albumin-bilirubin grade versus MELD score for predicting survival after
transjugular intrahepatic portosystemic shunt (TIPS) creation. Diagn Interv
Imaging
27. Xavier SA, Vilas-Boas R, Boal Carvalho P, Magalhães JT, Marinho CM, Cotter
JB (2018) Assessment of prognostic performance of Albumin–Bilirubin,
Child–Pugh, and Model for End-stage Liver Disease scores in patients with
liver cirrhosis complicated with acute upper gastrointestinal bleeding. Eur J
Gastroenterol Hepatol Publish Ahead of Print