BioMed Research International

BioMed Research International / 2020 / Article
Special Issue

Prognostic Assessment and Management of Liver Cirrhosis 2020

View this Special Issue

Clinical Study | Open Access

Volume 2020 |Article ID 5783748 | https://doi.org/10.1155/2020/5783748

Zhihui Duan, Li Li, Jinlong Li, Shengyun Zhou, "Validation of the Combined Model Based on Platelet Count and Albumin to Rule out High-Risk Varices in Liver Cirrhosis", BioMed Research International, vol. 2020, Article ID 5783748, 6 pages, 2020. https://doi.org/10.1155/2020/5783748

Validation of the Combined Model Based on Platelet Count and Albumin to Rule out High-Risk Varices in Liver Cirrhosis

Academic Editor: Xingshun Qi
Received29 Apr 2020
Revised06 Jun 2020
Accepted29 Jun 2020
Published13 Jul 2020

Abstract

Background. The Baveno VI criteria based on platelet count and liver stiffness, measured by transient elastography (TE), have been proposed to rule out high-risk varices (HRV) defined as medium or large-sized varices or the presence of high-risk stigmata (cherry red spots and red wale marks). However, TE is not available in all hospitals. Recently, the Rete Sicilia Selezione Terapia hepatitis C virus (RESIST-HCV) criteria recommended that cirrhotic patients with a and could avoid esophagogastroduodenoscopy (EGD) screening for HRV. Aim. We aimed to validate the performance of the RESIST-HCV criteria in two cohorts predominantly characterized with hepatitis B infection. Methods. Patients with compensated cirrhosis who had blood tests within three months of performing EGD and TE were enrolled retrospectively from two centers. RESIST-HCV criteria were applied to identify patients who did not require EGD screening. Results. This study included 188 patients from the Xingtai cohort (28 (14.9%) with HRV) and 104 patients from the Beijing cohort (19 (18.3%) with HRV). Of the patients who met the RESIST-HCV criteria (83 in the Xingtai cohort and 26 in the Beijing cohort), 0 and 1 had HRV, respectively, accounting for 44.1% (Xingtai cohort) and 25% (Beijing cohort) of endoscopies that were unnecessary. In the combined cohort, 109 (37.3%) patients met the RESIST-HCV criteria, only 1 (0.9%) HRV was missed, and the negative predictive value was 99.1%. Baveno VI and Expanded Baveno VI criteria spared 15.6% and 23.3% of EGDs, respectively, while missing 0% and 4.8% of HRV, respectively. Conclusions. In our population, the combined criteria based on platelet count and serum albumin performed well, saving 30-40% of EGDs and correctly identifying 99.1% of patients who could safely avoid screening endoscopies for high-risk varices in compensated cirrhotic patients.

1. Introduction

Portal hypertension (PH) is a common complication of liver cirrhosis, and it promotes the transition from the preclinical to the clinical phase of liver cirrhosis. Gastroesophageal varices (GEV) are a major and feared complication of PH, occurring in up to 60% of patients with cirrhosis [1]. Bleeding from GEV occurs as a severe and life-threatening complication of PH [2], with an extremely high risk of death. In particular, bleeding from GEV still has a mortality rate of 10%-15%, despite the clinical progress [3]. Prevention and treatment of variceal bleeding largely depends on the timely diagnosis and risk stratification of GEV [4, 5]. Esophagogastroduodenoscopy (EGD) remains the gold standard diagnostic method for GEV and should be performed to screen for the presence of GEV in all patients who are first diagnosed with liver cirrhosis, in accordance with the recent Baveno VI consensus [5]. However, a variable proportion of cirrhotic patients will not have GEV, as 30%-40% of all varices and 6%-20% of HRV are seen in compensated cirrhosis [3, 6]. Thus, screening all cirrhotic patients with EGD leads to a large number of unnecessary endoscopies, which increases the healthcare costs and the financial burden to the families and societies [7], and has a severe influence on the quality of life of patients. In addition, EGD is invasive, expensive, poorly accepted by patients, and unavailable in developing countries and rural areas [8]. Consequently, there have recently been significant updates in the noninvasive prediction of GEV, especially the use of noninvasive tests (NITs) to assess the likelihood of GEV and HRV [9]. NITs such as assessment of platelet count, spleen diameter, and liver stiffness can help identify patients at very low risk of having HRV or GEV [912]. Among them, the Baveno VI criteria ( kPa and /μL) are the most widely studied and employed, and these criteria are associated with<5% chance of missing HRV and can spare about 30% of EGD in compensated patients [5]. However, as transient elastography (TE) is not widely available in all liver units, the Baveno VI criteria cannot be applied in many clinical settings. The development of noninvasive criteria that do not include TE is desirable. Therefore, an easy-to-use Rete Sicilia Selezione Terapia hepatitis C virus (RESIST-HCV) criteria, which uses only platelet count and serum albumin, have been proposed to exclude HRV in compensated cirrhosis by Calvaruso et al. [13]. By using these criteria, the spared EGD rate and the missed HRV rate were 31.4% and 1.6%, respectively [13].

The primary aim of this study was to validate the performance and safety of the RESIST-HCV criteria compared to screening endoscopy for HRV. The secondary aim was to assess the performance of the Baveno VI and Expanded Baveno VI criteria.

2. Materials and Methods

2.1. Study Population

This was a retrospective study involving all patients with compensated cirrhosis who underwent EGD from January 2018 to January 2020 and who were referred to Xingtai People’s Hospital or Beijing Shijitan Hospital. The data collected included LSM (measured by TE), laboratory tests, liver ultrasonography findings, liver function tests, platelet counts, and EGD results.

2.2. Ethics

This study was conducted in compliance with the Declaration of Helsinki and approved by the Ethics Committees at Xingtai People’s Hospital and Beijing Shijitan Hospital. Given the retrospective nature of this study, obtaining informed consent was not applicable.

2.3. Inclusion Criteria

Patients with Child-Pugh A and B cirrhosis with NITs (laboratory tests, reliable LSM, and ultrasonography) performed within 3 months of EGD were included in the study. A diagnosis of cirrhosis was established based on the history of chronic liver disease, clinical manifestations (especially PH-related complications), liver and spleen ultrasonography and computed tomography findings, presence of GEV on EGD, , and previous liver biopsy if available.

2.4. Exclusion Criteria

Exclusion criteria were the occurrence of decompensation events (ascites, hepatic encephalopathy, Child-Pugh C, previous variceal bleeding, esophageal varices (EV) band ligation, portal vein thrombosis, transjugular intrahepatic portosystemic shunt, and hepatocellular carcinoma), current use of nonselective beta-blockers and antiplatelet agents, anticoagulation, and incomplete data.

2.5. Liver Stiffness Measurements

TE was only available for the Beijing cohort. LSM was assessed according to the manufacturer’s FibroScan standard procedure [14, 15], performed by one expert operator (Li Li) at Beijing Shijitan Hospital (>100 procedures). LSM was considered valid when there were at least 10 measurements with an [16]. Patients fasted for four hours before the procedure.

2.6. Upper Gastrointestinal Endoscopy

Two experienced endoscopists reviewed all the endoscopic findings and assessed the presence and size of GEV independently, without knowledge of the TE and blood test results and clinical data. The presence and size of EV were assessed according to the proposed guidelines [5]. Gastroesophageal varices were defined as low-risk varices (LRV) or high-risk varices (HRV). HRV were defined by a medium or large size or the presence of high-risk stigmata (cherry red spots and red wale marks) [5].

2.7. Laboratory Markers

Blood samples were drawn in the fasting state and handled according to the standard procedures of each hospital. The index blood samples chosen for assessing the proposed criteria were the closest to the screening endoscopy (within 3 months).

2.8. Statistical Analysis

Continuous data were all expressed as median with interquartile range (IQR), as none were normally distributed. Categorical data were expressed as numbers and percentages. A two-tailed value of less than 0.05 was considered statistically significant. LSM and laboratory data were compared between patients with and without HRV; continuous data were compared using Mann–Whitney test, and Fisher’s exact test was used for proportions for categorical data. The rate of spared EGD was calculated as the ratio of the numbers of patients with EGD that could be spared to the total number of patients. The missed HRV rate was defined by the rate of patients with missed HRV among the patients with spared EGD. Sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) were calculated. Statistical analysis was performed with the Statistical Package for Social Sciences (SPSS) version 20.0 (SPSS, Chicago, IL).

3. Results

3.1. Study Population

Over the study period, 137 compensated cirrhotic patients in the Beijing cohort and 248 patients from the Xingtai cohort underwent EGD. After excluding incomplete data, portal vein thrombosis, and unavailable lab tests within 3 months of EGD, a total of 292 patients from the two cohorts were included to validate the RESIST-HCV criteria, and 90 patients from the Beijing cohort were included to validate the Baveno VI and Expanded Baveno VI criteria. The flowchart of this study is shown in Figure 1. The baseline characteristics of the 292 patients with compensated cirrhosis are shown in Table 1. Overall, HRV was present in 16.1% (47 of 292 cases). The etiology of the underlying liver disease was hepatitis B virus (HBV) in 174 (59.6%), alcohol-related liver disease (ALD) in 12 (4.1%), primary biliary cholangitis (PBC) in 8 (2.7%), hepatitis C virus (HCV) in 4 (1.4%), and 93 others (31.8%); these others included unknown causes in 52, Budd-Chiari syndrome in 14, autoimmune hepatitis in 11, nonalcoholic fatty liver disease (NAFLD) in 9, drug reaction in 6, and overlap syndrome in 1. The majority of patients were Child-Pugh A (245; 83.9%), with 47 cases (16.1%) who were Child-Pugh B. In total, 90 patients had a reliable LSM from Beijing Shijitan Hospital. There were 109 (37.3%) patients who fulfilled the RESIST-HCV criteria ruling out the presence of HRV and could have avoided screening endoscopy. Only one patient with HRV was missed. The missed HRV rate was 0.9% and the NPV was 99.1%. The above data is summarized in Table 1. When compared to patients without HRV, those with HRV had lower platelet count (/L (/L) vs. /L (/L); ) and lower serum albumin (37.2 g/L (33.2-40.9 g/L) vs. 41.6 g/L (36.8-44.4 g/L); ), as seen in Table 2.


VariablesTotal cohort, Beijing cohort, Xingtai cohort,

Male (%)187 (64.0)57 (54.8)130 (69.1)
Age (years)52 (43-60.5)52 (43-60)52.5 (43-61.5)
BMI23.2 (21.4-25.2)23.2 (21.4-25.2)NA
Etiology
 Hepatitis B174 (59.6)36 (34.6)138 (73.4)
 Hepatitis C4 (1.4)0 (0)4 (2.1)
 PBC8 (2.7)5 (4.8)3 (1.6)
 Alcohol12 (4.1)11 (10.6)1 (0.5)
 Others93 (31.8)52 (50.0)41 (21.8)
Child-Pugh
 A245 (83.9)84 (80.8)161 (85.6)
 B47 (16.1)20 (19.2)27 (14.4)
Platelets (103/μL)111 (80-162.5)97 (68-139.5)118.5 (88.5-171)
ALT (IU/L)26.9 (19-41.9)22 (16-29.5)31.5 (21.3-50)
ALB (g/L)41 (36.3-44.1)37.5 (34.5-41.1)42.2 (38.5-45.7)
Bilirubin (μM/L)20.1 (14-30.1)21 (15.1-30.6)19 (14-28.8)
INR1.2 (1.1-1.3)1.2 (1.1-1.4)1.2 (1.1-1.3)
TE LSM (kPa)19.8 (12-34.8)19.8 (12-34.8)NA
High-risk varices (%)47 (16.1)19 (18.3)28 (14.9)
Any varices142 (48.6)54 (51.9)88 (46.8)
With RESIST-HCV criteria1092683
With RESIST-HCV criteria who had HRV110

Continuous variables are expressed as median (interquartile range) unless indicated. TE was available in 90 patients. Abbreviations: ALB: albumin; ALT: alanine aminotransferase; HRV: high-risk varices; INR: international normalized ratio; LSM: liver stiffness measurement; PBC: primary biliary cholangitis; TE: transient elastography.

VariablesHRV, Non-HRV,

Male (%)30 (63.8)157 (64.1)0.974a
Age (years)50 (44.5-58)53 (43-61)0.697
BMI22 (21.1-23.4)23.2 (21.5-25.2)0.126
Etiology0.363a
 Hepatitis B34140
 Hepatitis C04
 PBC17
 Alcohol210
 Others1083
Child-Pugh0.291a
 A37208
 B1037
Platelets (103/μL)77 (57.5-96)119 (90-169)<0.001
ALT (IU/L)29.3 (21-37)26.1 (18-42)0.465
ALB (g/L)37.2 (33.2-40.9)41.6 (36.8-44.4)<0.001
Bilirubin (μM/L)22.3 (15.5-33.2)20 (14-28.1)0.129
INR1.3 (1.2-1.4)1.2 (1.1-1.3)<0.001
TE LSM (kPa)30.1 (14-35.6)19.6 (12-34.8)0.405

Statistical comparison between the presence and absence of high-risk varices using Mann–Whitney test unless indicated. aStatistical comparison between the presence and absence of high-risk varices using Chi-square test or Fisher’s exact test. TE was available in 90 patients. Abbreviations: ALB: albumin; HCV: hepatitis C virus; INR: international normalized ratio; LSM: liver stiffness measurement; PBC: primary biliary cholangitis; TE: transient elastography.
3.2. Diagnostic Accuracy of RESIST-HCV Criteria for HRV

The RESIST-HCV criteria combine /μL and  g/L. In the combined cohort, 109 (37.3%) cases met these criteria, of whom 1 (0.9%) had HRV. Among the 183 (62.7%) cases that did not meet these criteria, 46 (25.1%) had HRV (Figure 2). The combination of platelet count and albumin using the recommended cut-off values to predict HRV gave a sensitivity of 97.9%, specificity of 44.1%, PPV of 25.1%, and NPV of 99.1% (Table 3). One case (0.9%) of HRV was missed (Figure 2), and the case had liver cirrhosis secondary to HBV, and the platelet count and albumin were 142000/μL and 40.5 g/L, respectively.


Pooled cohort (292patients)
CharacteristicsB6C ()EB6C ()RESIST-HCV ()

AUROC0.5990.6150.710
aSpared EGD, (%)14 (15.6)21 (23.3)109 (37.3)
bMissed HRV, (%)0 (0)1 (4.8)1 (0.9)
NPV (%)10095.299.1
Sen (%)10094.797.9
Spe (%)19.728.244.1
PPV (%)2526.125.1

Abbreviations: AUROC: area under receiving operator characteristics curve; B6C: Baveno VI criteria; EB6C: expanded Baveno VI criteria; EGD: esophagogastroduodenoscopy; HRV: high-risk varices; NPV: negative predictive value; PPV: positive predictive value; Sen: sensitivity; Spe: specificity. aThe spared EGD rate was calculated as the ratio between the number of patients with EGD that could be spared and the total number of patients. bThe missed HRV rate was defined as the rate of patients with missed HRV among the patients with spared EGD.
3.3. Analysis of the Avoidance of the Baveno VI, Expanded BavenoVI Criteria, and RESIST-HCV Criteria

Using the RESIST-HCV criteria, we classified all patients into low risk (those who fulfilled these criteria) and high risk (those who did not fulfill these criteria). The RESIST-HCV criteria could spare 37.3% (109 of 292) of EGDs, with a 0.9% (1 of 109) missed HRV rate and NPV of 99.1% (Table 3). Of the 90 patients who had reliable LSM from the Beijing cohort, 14 (15.6%) and 21 (23.3%) patients met the Baveno VI and the Expanded BavenoVI criteria, respectively, and 0% (0 of 14) and 4.8% (1 of 21) of HRV were missed, respectively. The RESIST-HCV criteria had the best performance with an area under receiving operator characteristics curve (AUROC) of 0.710 (Table 3).

4. Discussion

In the present study, we validated the recently published RESIST-HCV criteria [13] that use only platelet count and serum albumin level to identify patients who are at low risk of HRV and can safely avoid endoscopic screening, saving time and reducing costs. This is the first validation performed in Chinese patients. Interestingly, the main etiology of cirrhosis was HBV, which makes this study different from a previous study [13], where the main etiology was HCV. Compared with the study with HCV predominance, our study demonstrated that these criteria had a similar diagnostic accuracy for HBV-related cirrhosis patients. Applying these criteria in our study would have spared 37.3% of endoscopies, with a 0.9% missed HRV rate.

As expected, in our study, the RESIST-HCV criteria could safely avoid 37.3% (109 of 292) of EGDs, while maintaining the missed HRV rate below 5%, which was similar to the recent study by Calvaruso et al. [13]. In the large cohort of 1381 cirrhotic patients with HCV, the RESIST-HCV criteria spared 31.4% of EGDs and showed a 1.6% false-negative rate for the medium and large varices [13]. Similarly, the RESIST-HCV criteria failed to identify one (0.9%) HBV patient with HRV. To our knowledge, the RESIST-HCV criteria are clearly able and safe to stratify compensated cirrhotic patients for HRV risk. In the present study, the RESIST-HCV criteria were the most accurate diagnostic tool for ruling out HRV patients.

We further validated the Baveno VI and the Expanded Baveno VI criteria. In this study, the Baveno VI criteria were safe and 15.6% of patients could have avoided endoscopy, while the risk of missing HRV was 0%, and the NPV was 100%. The spared EGD rate (15.6%) was comparable with that reported in previous studies [7, 13, 1720]. In addition, our data demonstrated an acceptable rate of missing HRV. The Expanded Baveno VI criteria would have spared 23.3% of unnecessary EGDs and missed 4.8% of HRV. The number of spared EGDs is lower than the number reported in previous studies [7, 13, 14, 19]. The lower number of spared EGDs may be explained by the bias in selection of patients and the high prevalence of HRV, which may have led to a low NPV and influenced the diagnostic performance [18]. Besides, the sample size () is rather small. In addition, identifying and classifying varices in cirrhosis by different endoscopists may be inconsistent due to differences in technique and the experience of doctors [21].

Our study had a few limitations. First, the study was retrospective and the EV size and high-risk stigmata were evaluated by two experienced endoscopists. However, this issue was present in other studies [11, 13, 1820, 22]. Most studies that attempted to noninvasively rule out HRV, however, were retrospective and did not include an assessment of EV size [23]. Reassuringly, the diagnostic performance of the RESIST-HCV criteria was consistent with the performance reported in the recently published study [13]. Second, LSM measured by TE is useful for the assessment of HRV. However, TE was only available for 90 patients from Beijing Shijitan Hospital. Third, the present study lacked internal and external validation sets. Further validation in larger cohorts is needed.

5. Conclusions

Our study validated the RESIST-HCV criteria which could identify low-risk patients who can safely circumvent surveillance endoscopy for HRV screening for more than 30% of EGDs by using simple-to-use laboratory parameters not requiring TE. However, we have to acknowledge that a small proportion of HRV cases will be missed with an acceptable rate. Prospective validation of these criteria would be required to prove its diagnostic performance for HRV in other populations and various etiologies.

Abbreviations

ALT:Alanine aminotransferase
LSM:Liver stiffness measurement
TE:Transient elastography
HRV:High-risk varices
HCV:Hepatitis C virus
EGD:Esophagogastroduodenoscopy
PPV:Positive predictive value
NPV:Negative predictive value
pH:Portal hypertension
GEV:Gastroesophageal varices
NITs:Noninvasive tests.

Data Availability

The original data can be obtained from the correspondence author.

Ethical Approval

After review by the ethics committee, the health, rights, and privacy of the subjects were fully protected (approval letter no. 2020[017]).

Given the retrospective nature of this study and that all data were processed anonymously, obtaining an informed consent was not applicable.

Conflicts of Interest

All authors have no conflict of interest to disclose.

Authors’ Contributions

Zhihui Duan designed the study, collected data, analysed data, performed the statistical analyses, wrote the manuscript, and approved final manuscript. Li Li collected data, wrote the manuscript, and approved the final manuscript. Zhihui Duan and Li Li are co-first authors. Shengyun Zhou and Jinlong Li collected data and contributed to the drafting and final approval of the manuscript. Zhihui Duan and Li Li contributed equally to this work.

Acknowledgments

We thank the participants of the study. We would like to thank Editage (https://www.editage.cn) for English language editing.

References

  1. D. M. Jensen, “Endoscopic screening for varices in cirrhosis: findings, implications, and outcomes,” Gastroenterology, vol. 122, no. 6, pp. 1620–1630, 2002. View at: Publisher Site | Google Scholar
  2. G. D'Amico, G. Garcia-Tsao, and L. Pagliaro, “Natural history and prognostic indicators of survival in cirrhosis: a systematic review of 118 studies,” Journal of Hepatology, vol. 44, no. 1, pp. 217–231, 2006. View at: Publisher Site | Google Scholar
  3. G. Garcia-Tsao, A. J. Sanyal, N. D. Grace, W. D. Carey, Practice Guidelines Committee of American Association for Study of Liver Diseases, and Practice Parameters Committee of American College of Gastroenterology, “Prevention and management of gastroesophageal varices and variceal hemorrhage in cirrhosis,” The American Journal of Gastroenterology, vol. 102, no. 9, pp. 2086–2102, 2007. View at: Publisher Site | Google Scholar
  4. R. Franchis, “Non-invasive (and minimally invasive) diagnosis of oesophageal varices,” Journal of Hepatology, vol. 49, no. 4, pp. 520–527, 2008. View at: Publisher Site | Google Scholar
  5. R. Franchis and on behalf of the Baveno VI Faculty, “Expanding consensus in portal hypertension: report of the Baveno VI Consensus Workshop: stratifying risk and individualizing care for portal hypertension,” Journal of Hepatology, vol. 63, no. 3, pp. 743–752, 2015. View at: Publisher Site | Google Scholar
  6. M. Kovalak, J. Lake, N. Mattek, G. Eisen, D. Lieberman, and A. Zaman, “Endoscopic screening for varices in cirrhotic patients: data from a national endoscopic database,” Gastrointestinal Endoscopy, vol. 65, no. 1, pp. 82–88, 2007. View at: Publisher Site | Google Scholar
  7. G. Tosetti, M. Primignani, V. La Mura et al., “Evaluation of three "beyond Baveno VI" criteria to safely spare endoscopies in compensated advanced chronic liver disease,” Digestive and Liver Disease, vol. 51, no. 8, pp. 1135–1140, 2019. View at: Publisher Site | Google Scholar
  8. R. Lozano, M. Naghavi, K. Foreman et al., “Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010,” Lancet, vol. 380, no. 9859, pp. 2095–2128, 2012. View at: Publisher Site | Google Scholar
  9. S. S. Jakab and G. Garcia-Tsao, “Screening and surveillance of varices in patients with cirrhosis,” Clinical Gastroenterology and Hepatology, vol. 17, no. 1, pp. 26–29, 2019. View at: Publisher Site | Google Scholar
  10. E. Giannini, F. Botta, P. Borro et al., “Platelet count/spleen diameter ratio: proposal and validation of a non-invasive parameter to predict the presence of oesophageal varices in patients with liver cirrhosis,” Gut, vol. 52, no. 8, pp. 1200–1205, 2003. View at: Publisher Site | Google Scholar
  11. N. S. Ding, T. Nguyen, D. M. Iser et al., “Liver stiffness plus platelet count can be used to exclude high-risk oesophageal varices,” Liver International, vol. 36, no. 2, pp. 240–245, 2016. View at: Publisher Site | Google Scholar
  12. J. B. Maurice, E. Brodkin, F. Arnold et al., “Validation of the Baveno VI criteria to identify low risk cirrhotic patients not requiring endoscopic surveillance for varices,” Journal of Hepatology, vol. 65, no. 5, pp. 899–905, 2016. View at: Publisher Site | Google Scholar
  13. V. Calvaruso, I. Cacciola, A. Licata et al., “Is transient elastography needed for noninvasive assessment of high-risk varices? The REAL experience,” The American Journal of Gastroenterology, vol. 114, no. 8, pp. 1275–1282, 2019. View at: Publisher Site | Google Scholar
  14. M. I. Gaete, L. A. Díaz, A. Arenas et al., “Baveno VI and Expanded Baveno VI criteria successfully predicts the absence of high-risk gastro-oesophageal varices in a Chilean cohort,” Liver International, vol. 40, no. 6, pp. 1427–1434, 2020. View at: Publisher Site | Google Scholar
  15. J. Boursier, J. P. Zarski, V. de Ledinghen et al., “Determination of reliability criteria for liver stiffness evaluation by transient elastography,” Hepatology, vol. 57, no. 3, pp. 1182–1191, 2013. View at: Publisher Site | Google Scholar
  16. C. F. Dietrich, J. Bamber, A. Berzigotti et al., “EFSUMB guidelines and recommendations on the clinical use of liver ultrasound elastography, update 2017 (long version),” Ultraschall in der Medizin - European Journal of Ultrasound, vol. 38, no. 4, pp. e48–e48, 2017. View at: Publisher Site | Google Scholar
  17. P. Jangouk, L. Turco, A. de Oliveira, F. Schepis, E. Villa, and G. Garcia-Tsao, “Validating, deconstructing and refining Baveno criteria for ruling out high-risk varices in patients with compensated cirrhosis,” Liver International, vol. 37, no. 8, pp. 1177–1183, 2017. View at: Publisher Site | Google Scholar
  18. A. Colecchia, F. Ravaioli, G. Marasco et al., “A combined model based on spleen stiffness measurement and Baveno VI criteria to rule out high-risk varices in advanced chronic liver disease,” Journal of Hepatology, vol. 69, no. 2, pp. 308–317, 2018. View at: Publisher Site | Google Scholar
  19. S. Petta, G. Sebastiani, E. Bugianesi et al., “Non-invasive prediction of esophageal varices by stiffness and platelet in non-alcoholic fatty liver disease cirrhosis,” Journal of Hepatology, vol. 69, no. 4, pp. 878–885, 2018. View at: Publisher Site | Google Scholar
  20. H. A. Lee, S. U. Kim, Y. S. Seo et al., “Prediction of the varices needing treatment with non-invasive tests in patients with compensated advanced chronic liver disease,” Liver International, vol. 39, no. 6, pp. 1071–1079, 2019. View at: Publisher Site | Google Scholar
  21. A. Cardenas and J. G. Abraldes, “Classifying varices in cirrhosis: who’s got the best look?” Liver International, vol. 40, no. 4, pp. 754-755, 2020. View at: Publisher Site | Google Scholar
  22. X. Qi, Y. Li, R. Wang et al., “Liaoning score for prediction of esophageal varices in cirrhotic patients who had never undergone endoscopy: a multicenter cross-sectional study in Liaoning Province, China,” Advances in Therapy, vol. 36, no. 8, pp. 2167–2178, 2019. View at: Publisher Site | Google Scholar
  23. L. Castera, “Transient elastography and other noninvasive tests to assess hepatic fibrosis in patients with viral hepatitis,” Journal of Viral Hepatitis, vol. 16, no. 5, pp. 300–314, 2009. View at: Publisher Site | Google Scholar

Copyright © 2020 Zhihui Duan 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.


More related articles

 PDF Download Citation Citation
 Download other formatsMore
 Order printed copiesOrder
Views273
Downloads301
Citations

Related articles

Article of the Year Award: Outstanding research contributions of 2020, as selected by our Chief Editors. Read the winning articles.