248

ORIGINAL
Non-invasive assessment of large esophageal varices withliver cirrhosis ; a study conducted in Pakistan
Khalid Mahmood1, Iftikhar Haider2, Syed Omair Adil3, Muhammad Ubaid4, and Abu Talib2
Former Dean, Department of Medicine and Allied Sciences, Dow University of Health Sciences, Karachi, Pakistan, 2Department of Medicine,Dow University of Health Sciences, Karachi, Pakistan, 3Department of Research, Dow University of Health Sciences, Karachi, Pakistan,
4
Medical Unit I, Civil Hospital Karachi, Pakistan
1

Abstract : The assessment of non-invasive parameters for the prediction of large esophageal varices among patientswith liver cirrhosisis is of utmost importance. In this study, non-invasive parameters for prediction of large
esophageal varices were retrospectively evaluated. The presence of esophageal varices grade III and IV was classified
as large esophageal varices positive while no varices or grade I and II were classified as large esophageal varices
negative. There were 473 (90.09%) patients with ascites [mild 38 (8.03%), moderate 257 (54.33%) and severe 178(37.63%)]. Frequency of esophageal varices was found to be higher (n=415, 79.04%). Whereas, large esophageal
varices were found in 251 (47.81%) patients. The sensitivity, specificity, positive predicted value, negative predictedvalue and test accuracy of thrombocytopenia in predicting large esophageal varices were found to be 88.05%,
59.85%, 66.77%, 84.54% and 73.33% respectively. A significant association for large esophageal varices wasobserved for low platelet counts (AOR : 0.98, 95% CI : 0.97-0.99), high bilirubin level (AOR : 1.22, 95% CI : 1.07-1.39),
ascites (AOR : 1.98, CI : 1.02-3.85) and Child score A (AOR : 0.26, 95% CI : 0.09-0.75) and Child Score B (AOR : 0.42,
95% CI : 0.28-0.61). In conclusion, low platelet count, high bilirubin level and ascites are found to be non-invasive
predictive factor for large esophageal varices. J. Med. Invest. 66 : 248-251, August, 2019
Keywords : Large esophageal varices (LEVx), Platelet, Bilirubin, Liver cirrhosis

INTRODUCTION
Esophageal varices are a big challenge in managing cirrhotic
patients and suggest its early detection with either invasive or
non-invasive methods. (1)Various studies have evaluated the non-invasive predicting
markers for large esophageal varices (LEVx) (2-5). Advanced
Child-Pugh score, platelet count, serum albumin level, splenomegaly and increase portal vein diameter at ultrasonography
are reported by several studies as the possible useful markers(6-8).It is stated that due to the disparities in the etiology
and severity of liver cirrhosis and because of the nutritional
status differences, these non-invasive prognostic factors showedvariations when studied in different populations (8). Frequenthospitalizations due to the complications including the variceal
bleeding are owing to late presentation of cirrhotics in our country (9).
American Association for the Study of Liver Disease (AASLD)
and American College of Gastroenterology (ACG) practice guidelines have stated that upper GI endoscopy should be performed
in all patients with liver cirrhosis to rule out LEVx. If the patient
is found positive for having LEVx, treatment with β-adrenergic
receptor antagonists should be started (10). Though long-term
administration of β-adrenergic receptor antagonists in patientswith LEVx reduces the incidence of first variceal bleeding,adverse effects are largely reported from its prolonged administration (11). In addition, its use is not recommended in patientswith small esophageal varices (11, 12).
Received for publication September 6, 2018 ; accepted March 1, 2019.
Address correspondence and reprint requests to Syed Omair Adil,
Lecturer, Department of Research, Dow University of Health Sciences,
Gulzar-e-Hijri, Ojha Campus, Suparco Road, KDA Scheme-33,
Karachi, Pakistan and Fax : +923322319119.

Consequently, LEVx screening not only generates a hugeburden on endoscopic units but is also a financial constraint onliver cirrhotics. Keeping the social, financial, and healthcare
resource burdens implicated by these recommendations, recent
studies have focused on the utility of non-invasive approaches to
identify patients with LEVx, thereby, preventing the endoscopyof patients with lower risk (3-5, 8).

METHODOLOGY
A retrospective study at Civil Hospital Karachi (CHK) was
conducted from 2012 to 2016 after taking ethical approval (IRB878/DUHS/2017/78) from Dow University of Health Sciences(DUHS).

Diagnosis
Cirrhosis was confirmed on clinical (stigmata of chronic liverdisease), biochemical and radiological (abdominal ultrasound orcomputerized tomography) parameters. Radiological features
demonstrated small shrunken liver and intra-abdominal varices
with or without enlarged spleen. Cirrhosis was also confirmed ona histopathological basis, wherever required (13).
Gastroesophageal varices were defined and classified in accordance to Dagradi classification (14). Varices with blue or red incolor and brought out by compression of the esophageal wall withthe tip of the oesophagoscope were defined as grade 1. Grade 1
varices are usually linear, maybe sigmoid shaped having lessthan 2 mm in diameter. Grade 2 varices were defined as bluish,
mildly tortuous or straight, and were elevated above the surface
or the relaxed esophagus having 2-3 mm in diameter. Grade 3
were vividly elevated bluish veins either straight or tortuous
having 3-4 mm in diameter. Tortuous bluish varices having > 4
mm in diameter, which completely occupies the esophageal
lumen closely packed around the wall and may or may not have

The Journal of Medical Investigation Vol. 66 2019

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The Journal of Medical Investigation Vol. 66 August 2019a good mucosal cover defined as Grade 4. Varices grape-like inappearance, obstructing the lumen of the approaching oesophagoscope with presence of small, cherry-red varices overlying thelarge, slightly deeper lying, slate blue-grey varices (also known
as ‘varices over varices’) were defined as grade 5.
Those patients with the presence of hepatocellular carcinoma(HCC), portal hypertension surgery, history of esophageal variceal bleeding, on primary prophylaxis treatment for variceal
bleeding, sclerotherapy and/or portal vein thrombosis (PVT)
were excluded to control the factors affecting the platelet count.

Data collection
A detailed demographic and clinical information including
age, gender, hematological and biochemical findings, liver disease severity, and ascites were recorded. The severity of the liverdisease was noted on the basis of Child-Pugh Score whereas
ascites was graded as none, mild, moderate and severe. Laboratory findings were evaluated using hemoglobin (Hb) count,platelet count, total leukocyte count (TLC), serum concentrationof albumin, bilirubin, alkaline phosphate (ALP), and alanine
aminotransferase (ALT). The seropositivity of hepatitis B and C
virus were also evaluated with patient’s history of alcohol intake
and intravenous drug abuse.
Abdominal ultrasonography with high-resolution real-time ultrasound machines was performed in all patients using GE Voluson S8 and Xario 100, Toshiba using 3.5-MHz convex transducer.
Endoscopy of the upper gastrointestinal system was performed
using one endoscopic unit (Olympus Corporation, Tokyo, Japan).
The presence of esophageal varices grade III & IV was classified as LEVx positive while no varices or grade I & II wereclassified as LEVx negative.

Statistical analysis
The mean and standard deviation for quantitative variables
like age, Hb level, platelets count, TLC, Albumin, Bilirubin, ALP,
and ALT was calculated while frequency and percentages forquantitative variables like gender, ascites, and the Child-Pughscore were calculated. Differences in the mean values of quantitative variables were explored using independent t-test while tocheck the relationship in between LEVx and quantitative variables, chi-square test was applied. P-value < 0.05 was consideredsignificant.
The significant association between various independent
variables and outcome variable (LEVx) were also explored using
univariate binary logistic regression. All significant variables
in univariate analysis were selected for multiple logistic regressions to calculate adjusted odds ratio (AOR).
Diagnostic accuracy was calculated using the standard thrombocytopenia level (150,000) as cut-off point of platelets counts.

RESULTS
Initially, 600 patients were included. However, 75 patientswere excluded because of the presence of HCC and/or history ofesophageal variceal bleeding and portal vein thrombosis. Thus,in the final analysis, 525 cases were selected. The mean age wasreported as 46.44 ± 14.43 years. Majority of the patients (n = 279,
53.14%) were males. HCV virus was the predominant hepatic
cirrhosis etiology reported in 396 (75.42%) patients, whereas
HBV virus was found in 57 (10.85%), Cryptogenic 41 (7.81%),
Wilson’s Disease 14 (2.67%), autoimmune hepatitis 9 (1.71%),
alcoholism 5 (0.95%), and both HBV and HCV were found in 3
(0.57%) patients. There were 473 (90.09%) patients with ascites.
Among these, mild ascites was observed in 38 (8.03%), moderate
in 257 (54.33%) and severe in 178 (37.63%) patients.

The endoscopic finding showed that esophageal varices were
found in 415 (79.04%) patients. Out of these 415 esophageal varices positive patients, “grade I” esophageal varices were observedin 48 (11.56%) patients, “grade II” in 116 (27.97%), “grade III” in
202 (48.67%), and “grade IV” in 49 (11.81%) patients. There were251 (47.81%) patients with LEVx (grade III & IV) whereas 274(52.19%) patients with no LEVx.
The Child-Pugh score C was found in the majority (n = 328,
62.47%) of the patients followed by Child-Pugh Score B in 178(33.90%) and Child-Pugh score A in 19 (3.62%) patients.
Thrombocytopenia (platelet count below 150,000) was observed in 331 (63.04%) patients whereas 194 (36.95%) patientswere presented with normal platelet count (platelet count above
150,000). A significant difference of esophageal varices wasobserved among patients with and without thrombocytopenia(p-value < 0.001). LEVx was found significantly higher (n = 221,66.8%) among patients with thrombocytopenia as compared tonormal platelet count (n = 30, 15.5%) (p-value < 0.001). (Figure
1) The sensitivity, specificity, PPV, NPV and test accuracy ofthrombocytopenia in predicting LEVx was found to be 88.05%,
59.85%, 66.77%, 84.54% and 73.33% respectively. (Table I)
The difference in majority of the variables were insignificant
among patients with and without LEVx including age (p-value
0.092), gender (p-value 0.442), Hb (p-value 0.175), TLC (p-value
0.159), ALP (p-value 0.202), and ALT (p-value0.075). While, theplatelet count (p-value < 0.001), Bilirubin (p-value < 0.001), presence of ascites (p-value 0.045) and Child-Pugh Score (p-value <0.001) were the only variables found significantly related with
LEVx. (Table II)
The univariate analysis revealed that platelet counts(OR : 0.98, 95% CI : 0.97-0.99),Child score A (OR : 0.28, 95%
CI : 0.98-0.79) and Child Score B (OR : 0.42, 95% CI : 0.29-0.61)

Figure 1 : Difference between occurrence of large size esophageal
varices versus no large size esophageal varices in thrombocytopenic
and non-thrombocytopenic patients (n = 525)
Table I : Diagnostic accuracy of thrombocytopenia in predicting
large esophageal varices (n = 525)
Thrombocytopenia
Yes

Large scale esophageal varices
Yes

No

Total

221

110

331

No

30

164

194

Total

251

274

525

Sensitivity : 88.05%
Specificity : 59.85%
Positive Predicted Value (PPV) : 66.77%
Negative Predicted Value (NPV) : 84.54%
Test Accuracy : 73.33%

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K. Mahmood, et al. Non-invasive assessment of esophageal varices

were less likely whereas bilirubin level (OR : 1.18, 95% CI : 1.061.31) and presence of ascites (OR : 1.83, 95% CI : 1.01-3.34) weremore likely to have LEVx. Similarly, on multivariate analysis(adjusted for platelet counts, bilirubin, ascites and Child-Pughscore), platelet counts (AOR : 0.98, 95% CI : 0.97-0.99),Childscore A (AOR : 0.26, 95% CI : 0.09-0.75) and Child Score B(AOR : 0.42, 95% CI : 0.28-0.61) were less likely whereas bilirubin level (AOR : 1.22, 95% CI : 1.07-1.39) and presence of ascites(AOR : 1.87, 95% CI : 1.02-3.49) were more likely to have LEVx.
(Table III)
Table II : Comparison of Large esophageal varices with predictor
variables (n = 525)
Variables

Large esophageal varices (LEVx)
Positive
Negative(n=251)(n=274)p-valuen (%)
n (%)
45.33 ±14.37
47.46 ±14.43
0.092†

Age (years)
GenderMale
150 (53.8)
129 (46.2)
Female124 (50.4)
122 (49.6)
Hematological and biochemical findings
Hb (g/dl)
7.05 ±0.83
7.14 ±0.73
TLC (x 1000/μL)
7.17 ±5.32
7.92 ±6.73
Platelets (x 1000/μL) 67.07 ±35.47
183.57 ±158.78
Albumin (mg/dL)
2.77 ±0.452.69 ±0.46
Bilirubin (mg/dL)
2.23 ±2.07
1.73 ±1.35
ALP (IU/L)
71.47 ±42.57
67.01 ±37.43
ALT (IU/L
225.76 ±109.99 206.89 ±130.52
AscitesYes
233 (49.3)
240 (50.7)
No
18 (34.6)
34 (65.4)
Child-Pugh ScoreA
5 (26.3)
14 (73.7)
B
62 (34.8)
116 (65.2)
C
184 (56.1)
144 (43.9)†

0.442‡
0.175†
0.159†<0.001†**
0.056†<0.001†**0.202†
0.075†
0.045‡*<0.001‡**

Independent t-test applied, ‡Chi-square test applied, *p-value < 0.05,**p-value < 0.001

ALP : Alkaline Phosphate, ALT : Alanine Transaminase, TLC :Total Leukocyte Count, Hb : Hemoglobin

Table III : Regression analysis of factors associated with large esophageal
varices (n = 525)
OR (95% CI)
p-value AOR (95% CI) p-valueAge (years)
0.99 (0.97-1.01) 0.092
GenderMale
0.874 (0.62-1.23) 0.442
Female1
Hematological and biochemical findings
Hb (g/dl)
0.85 (0.69-1.07) 0.175
TLC (x 1000/μL)
0.98 (0.95-1.01) 0.159
Platelets (x 1000/μL) 0.98 (0.97-0.99) <0.001 0.98 (0.97-0.99) <0.001
Albumin (mg/dL)
1.44 (0.98-2.09) 0.057
Bilirubin (mg/dL)
1.18 (1.06-1.31) <0.001 1.22 (1.07-1.39) 0.003
ALP (IU/L)
1.01 (0.99-1.02) 0.202
ALT (IU/L)
0.99 (0.99-1.01) 0.120
AscitesYes
1.83 (1.01-3.34) 0.047
1.87 (1.02-3.49) 0.040No11Child-Pugh Score
A
0.28 (0.98-0.79) 0.017
0.26 (0.09-0.75) 0.0.12
B
0.42 (0.29-0.61) <0.001 0.42 (0.28-0.61) <0.001
C1
1
CI : Confidence Interval, OR : Odds ratio, AOR : Adjusted Odds Ratio,
ALP : Alkaline Phosphate, ALT : Alanine Transaminase, TLC : Total
Leukocyte Count, Hb : Hemoglobin

DISCUSSION
This study has shown a higher proportion of patients withliver cirrhosis having LEVx. Low platelet counts, high bilirubinlevel, presence of ascites, severity of cirrhosis (CTP-A, and CTPB) were found to have predictive ability on univariate analysis.
Earlier studies (2, 4, 15-17) have also shown an independent
predictive ability of low platelet count in liver cirrhosis patientsto predict LEVx.
A palpable or enlarged spleen is reported to be an important
predictor in most of the studies (2, 6, 18-20). Various studies haverecommended “platelet count/spleen diameter” (PC/SD) ratio as
the most viable non-invasive tool in the prediction of the varices(4, 19-23). However, as this study is retrospective PC/SD ratio of
our patients was not calculated. Though mostly earlier studies
have shown PC/SD ratio as an effective non-invasive parameterfor prediction of LEVx, but one local study in Pakistan has shown
contrary findings (24) where PC/SD ratio could not reliably predict the esophageal varices in cirrhotic patients. Furthermore,
above referred study (24) have also reported an insignificant
association of low platelet count with esophageal varices.
Low platelet count and ascites are widely reported as a noninvasive predictor of esophageal varices by earlier published studies (25-31) which is in agreement to this study. Prior studies (32,33) have validated both clinical and sonologically determined
ascites as an independent predictor for LEVx.
High level of serum bilirubin has shown a significant predictor for LEVx in this study which is in accordance to an earlier
study (29). Schwarzenberger et al. in their study reported various
parameters like ascites, splenomegaly, serum albumin concentration, Child score, and portal vein diameter as predictive variables for LEVx (30). Recently, Chen et al evaluated the combined
effect of “albumin bilirubin grade and platelet count” to predictrisk of large varices and variceal haemorrhage (5). Due to thediversity of liver diseases and variations in the characteristics
among different populations earlier studies have shown different
parameters to predict large esophageal varices. In fact, a highly
accurate non-invasive predictive model for LEVx is still awaited(4).
Findings of this study could be ascertained in the light of thelimitations that due to retrospective nature of the study, spleen
diameter values of our patients were not collected. Thus, PC/
SD ratio of our patients was not evaluated which if determined
would have a more statistical impact. However, to the best of ourknowledge, this is the first study from Pakistan reporting thepredicting factor for LEVx from such a larger population.

CONCLUSION
Low platelet count, high bilirubin level and presence of ascites
can be used as independent non-invasive predictive factors for
LEVx among patients with liver cirrhosis. Further validation ofthese non invasive parameters through large prospective studies
in resource-limited areas like Pakistan where endoscopy is notavailable everywhere,would definitely provide a non invasive
alternative to endoscopy with substantial reduction in financial
burden.

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