Skip to content

Advertisement

BMC Gastroenterology

Research article
Open Access
Open Peer Review

This article has Open Peer Review reports available.

How does Open Peer Review work?

Portal hypertensive gastropathy as a prognostic index in patients with liver cirrhosis

  • Chang Seok Bang†1,
  • Hyo Sun Kim†1,
  • Ki Tae Suk1,
  • Sung Eun Kim1,
  • Ji Won Park1,
  • Seung Ha Park2,
  • Hyoung Su Kim1,
  • Myoung Kuk Jang1,
  • Sang Hoon Park1,
  • Myung Seok Lee1,
  • Choong Kee Park1 and
  • Dong Joon Kim1Email author
†Contributed equally
BMC GastroenterologyBMC series – open, inclusive and trusted201616:93

https://doi.org/10.1186/s12876-016-0508-2

©  The Author(s). 2016

Received: 1 March 2016

Accepted: 2 August 2016

Published: 12 August 2016

Open Peer Review reports

Abstract

Background

Portal hypertensive gastropathy (PHG) is a frequently overlooked complication of liver cirrhosis (LC). The clinical implications of PHG as a prognostic factor of LC or a predictive factor for the development of hepatocellular carcinoma (HCC) have not been established. The aim of this study was to assess the clinical significance of PHG in patients with LC.

Methods

Patients with LC were prospectively enrolled and followed in a single tertiary hospital in the Republic of Korea. Baseline hepatic vein pressure gradient (HVPG) was measured, and esophagogastroduodenoscopy (EGD) was performed. The associations of PHG with HVPG, survival and the development of HCC were evaluated.

Results

A total of 587 patients were enrolled. The mortality rate was 20.3 % (n = 119), and HCC developed in 9.2 % (n = 54) during the follow-up period (32.6 ± 27.8 months). The grade of PHG was well correlated with HVPG (no PGH: median 9.2 [IQR: 7.2–16.7], mild PHG: 14.6 [10.1–19.3], and severe PHG: 17.3 [12.3–21.5], P < 0.001), as well as with Child-Pugh class, MELD score or survival. However, it was not associated with the development of HCC. The grade of PHG (HR 3.29, 95 % CI: 1.12–9.63, severe vs. no PHG) and Child-Pugh class (HR 3.53, 95 % CI: 1.79–6.97, Child C vs A) showed significant associations with mortality.

Conclusion

PHG was well correlated with portal hypertension and could be used as a prognostic factor for LC but not for the prediction of HCC.

Keywords

CirrhosisPortal hypertensionPortal hypertensive gastropathyHepatocellular carcinoma

Background

Portal hypertension is a complication of liver cirrhosis (LC) and the main pathophysiologic mechanism that potentiates various adverse gastrointestinal consequences, including esophageal or gastric varices, gastropathy, and enteropathy [1, 2].

Portal hypertensive gastropathy (PHG) is a frequently overlooked complication in patients with LC. More attention has been focused on the detection or evaluation of esophageal or gastric varices by endoscopists. This complex secondary change in the gastric mucosa resulting from portal hypertension is a potential cause of acute or chronic hemorrhage [3]. It can also be severe and fatal, although less frequently than variceal hemorrhage [4].

In addition to the potential hemorrhagic focus, the clinical implications of PHG have not been well established. Previous studies have also shown conflicting results regarding the correlation between PHG and the severity of liver disease [5–13]. The aim of this study was to evaluate the clinical implications of PHG as a prognostic factor of LC or a predictive factor for the development of hepatocellular carcinoma (HCC) in patients with LC.

Methods

Patients

Patients with chronic liver disease were prospectively enrolled and followed in a single tertiary hospital in the Republic of Korea. Baseline hepatic vein pressure gradient (HVPG) was measured, and esophagogastroduodenoscopy (EGD) was performed in all consecutive patients for the detection or evaluation of the severity of PHG. Both procedures were performed consecutively and the time interval between 2 procedures was minimal. Patients without LC or with incomplete data were excluded from this study. The clinical and endoscopic characteristics of patients with LC were reviewed and analyzed. Data were recorded for the following variables: sex, age, the etiology of LC, endoscopic findings, laboratory findings, and HVPG. Laboratory findings including Child-Pugh classification and Model for End-stage Liver disease (MELD) score were assessed based on hospitalization day.

Differentiation of etiology

The differentiation between LC and chronic hepatitis relied on clinical, laboratory, radiologic and histologic information. The final determination of LC was made by two hepatologists (K.T.S and D.J.K).

In terms of the etiology, chronic hepatitis B was defined as positive for hepatitis B surface antigen (HBsAg) with abnormal levels of aspartate transaminase (AST) / alanine transaminase (ALT) for a period longer than 6 months. Chronic hepatitis C was defined as positivity for hepatitis C antibodies (Anti-HCV) and serum RNA (HCV-RNA) with abnormal levels of AST/ALT for a period longer than 6 months. Determination of alcoholic hepatitis used history of alcohol abuse (>40 g/day for men, >20 g/day for women) [14, 15], physical findings (delirium tremens or alcohol withdrawal seizure), laboratory tests (AST/ALT >2, elevated level of gamma glutamyl transpeptidase, or enlarged mean corpuscular volume), or liver biopsy (steatosis, hepatocyte ballooning, Mallory-Denk bodies, megamitochondria, canalicular and/or lobular bilirubinostasis, or polymorphonuclear neutrophil infiltration), after excluding other potential etiologies. The determination of non-alcoholic steatohepatitis relied on history (exclusion of significant alcohol consumption), laboratory tests (AST or ALT elevation), imaging modalities (hepatic steatosis), or liver biopsy (macrovesicular fatty changes, hepatocyte ballooning, or inflammatory cell infiltrate), after excluding other potential etiologies.

Endoscopy and HVPG measurement

PHG was evaluated by EGD performed by 6 experienced endoscopists (>6000 cases of endoscopy). The diagnosis and determination of degree were based on the Baveno III scoring system [16]. To minimize the inter-observer variability, all of the endoscopic data and diagnoses were reviewed by 6 experienced endoscopists. Cases of disagreement were discussed and resolved by consensus, according to the Baveno III scoring system. To exclude single gastric antral vascular ectasia cases, not relevant to portal hypertension, authors categorized enrolled population according to the presence of PHG or not (binary criteria), in addition to the Baveno III scoring system for PHG, and six experienced endoscopists made decisions by consensus.

HVPG was measured with transjugular access under fluoroscopic guidance by 2 experienced hepatologists (K.T.S and S.H.P >300 cases of HVPG measurements). A catheter was placed into one of the hepatic vein branches, and the pressure was measured three times using the ballooning and deballooning method of the hepatic vein. The average number was recorded and decided upon as the patient’s HVPG. Informed consent was obtained. Vital signs were continuously monitored, and the patients were observed carefully to detect the development of serious complications during and after the measurement of HVPG.

Statistical analysis

Continuous variables are expressed as the medians and interquartile ranges (IQRs) because they were not normally distributed. Categorical variables are expressed as numbers and percentages. The Mann-Whitney test and Fisher’s exact test were used to compare two variables. The Kruskal-Wallis test and Fisher’s exact test were used to evaluate the three study arms. Post hoc analysis was performed using Bonferroni’s correction. Survival analysis, including the development of HCC, was performed using the Kaplan-Meier method and the log rank test. The Cox proportional hazard model was applied for the detection of associated factors for survival and the development of HCC. A P value < 0.05 (2-tailed) was adopted as the threshold of statistical significance for all of the tests. The analysis was performed using SPSS software, version 21.0 (SPSS Inc., Chicago, IL, USA). All of the authors had access to the study data and reviewed and approved the final manuscript.

Results

Characteristic of patients

Between January 2006 and May 2013, 1002 patients were initially enrolled. Patients without LC or with incomplete data were excluded from this study. The number of excluded cases from each category was as follows: no LC (n = 373), incomplete endoscopic evaluation (n = 37), and incomplete HVPG measurement (n = 5). Finally, 587 patients were included in the analysis of this study (Fig. 1).
Fig. 1

Flow diagram of study design

The clinical characteristics of these patients are summarized in Table 1. The median age was 51 years old (IQR: 45–59) in the total population. Male predominance was observed in the collected data for 78.7 % of the total patients. In terms of the etiology, alcohol abuse was the most frequent cause of LC (69.8 %), followed by hepatitis B virus (HBV) infection (24.2 %), hepatitis C virus (HCV) infection (5.8 %), and non-alcoholic causes (0.2 %).
Table 1

Clinical characteristics of total patients

Characteristics, N (%)

Total (N = 587)

Age (years), Median (Interquartile range)

51 (45–59)

Sex

Male

462 (78.7 %)

Female

125 (21.3 %)

Etiology

Alcohol

410 (69.8 %)

HBV

142 (24.2 %)

HCV

34 (5.8 %)

Non-alcoholic

1 (0.2 %)

PHG

No PHG

50 (8.5 %)

Mild PHG

411 (70 %)

Severe PHG

126 (21.5 %)

Child-Pugh classification

Class A

283 (48.2 %)

Class B

234 (39.9 %)

Class C

70 (11.9 %)

HVPG (mmHg), Median (Interquartile range)

14.8 (10–20)

MELD score

9.3 (6.0–13.0)

Albumin (g/dL)

3.3 (2.8–3.8)

Total bilirubin (mg/dL)

1.4 (0.8–2.7)

Platelet count (x 103/mL)

105 (74–160)

Prothrombin time (INR)

1.26 (1.11–1.44)

Follow-up duration (months), Mean ± SD

32.59 ± 27.77

Survival

468 (79.7 %)

HCC

54 (9.2 %)

N number, HBV hepatitis B virus, HCV hepatitis C virus, PHG portal hypertensive gastropathy, HVPG hepatic vein pressure gradient, MELD model for end-stage liver disease, INR international normalized ratio, SD standard deviation, HCC hepatocellular carcinoma

Regarding the severity of LC, approximately half of the patients were included in Child-Pugh classification A (48.2 %), followed in order by B (39.9 %) and C (11.9 %). The median value of HVPG was 14.8 (IQR: 10–20), and the MELD score was 9.3 (IQR: 5.7–13.0).

PHG was detected in 91.5 % of the patients. Among the patients with PHG, the severe category constituted 21.5 %, and 70 % of the patients showed mild PHG. Patients with only gastric antral vascular ectasia was 3 (0.51 %). During the follow-up period (32.59 ± 27.77 months), the overall survival rate was 79.7 %, and 9.2 % of the patients developed HCC. The proportion patients lost to follow-up was 12.8 % (n = 75).

There were no serious complications during or after HVPG measurements. Transient ventricular premature contraction was frequently noted when the tip of the measurement catheter passed the right atrium. Cardiac rhythm recovered without any treatment after a few seconds.

Univariate analysis for PHG

The univariate analyses for PHG in LC are listed in Tables 2 and 3. There were significant differences in the distributions of Child-Pugh classification, HVPG, and MELD score, as well as laboratory parameters, between patients with and without PHG (Table 2). In the analysis stratified by the severity of PHG (no PHG vs mild PHG vs severe PHG), this finding was consistent (Table 3).
Table 2

Univariable analysis for PHG in patients with liver cirrhosis

Variables, N (%)

No PHG

PHG

P value

N = 50 (8.5 %)

N = 537 (91.5 %)

Age (years), Median (Interquartile range)

52 (43–60.25)

51 (45–59)

0.64

Sex

  

0.002

Male

30 (60 %)

432 (80.4 %)

Female

20 (40 %)

105 (19.6 %)

Etiology

  

<0.001

Alcohol

20 (40 %)

390 (72.6 %)

HBV

26 (52 %)

116 (21.6 %)

HCV

4 (8 %)

30 (5.6 %)

Non-alcoholic

0 (0 %)

1 (0.2 %)

Child-Pugh classification

  

<0.001

Class A

37 (74 %)

246 (45.8 %)

Class B

12 (24 %)

222 (41.3 %)

Class C

1 (2 %)

69 (12.8 %)

HVPG (mmHg), Median (Interquartile range)

9.2 (7.23–16.73)

15 (11–20)

<0.001

MELD score

6.00 (6.00–8.07)

9.83 (6.00–13.58)

<0.001

Albumin (g/dL)

3.7 (3.0–4.1)

3.2 (2.8–3.7)

0.001

Total bilirubin (mg/dL)

0.9 (0.6–1.2)

1.5 (0.9–2.9)

<0.001

Platelet count (x 103/mL)

141.5 (94.8–214.3)

104 (71–157)

0.001

Prothrombin time (INR)

1.12 (1.04–1.32)

1.28 (1.12–1.45)

<0.001

Survival

46 (92 %)

422 (78.6 %)

0.004

HCC

5 (10 %)

49 (9.1 %)

0.33

N number, HBV hepatitis B virus, HCV hepatitis C virus, PHG portal hypertensive gastropathy, HVPG hepatic vein pressure gradient, MELD model for end-stage liver disease, INR international normalized ratio, SD standard deviation, HCC hepatocellular carcinoma

Table 3

Univariable analysis for PHG in patients with liver cirrhosis

Variables, N (%)

No PHG

Mild PHG

Severe PHG

P value

N = 50 (8.5 %)

N = 411 (70 %)

N = 126 (21.5 %)

Age (years), Median (Interquartile range)

52 (43–60.25)

52 (46–60)

51 (45–56)

0.24

Sex

   

0.001

Male

30 (60 %)

324 (78.8 %)

108 (85.7 %)

Female

20 (40 %)

87 (21.2 %)

18 (14.3 %)

Etiology

   

<0.001

Alcohol

20 (40 %)

284 (69.1 %)

106 (84.1 %)

HBV

26 (52 %)

99 (24.1 %)

17 (13.5 %)

HCV

4 (8 %)

27 (6.6 %)

3 (2.4 %)

Non-alcoholic

0 (0 %)

1 (0.2 %)

1 (0 %)

Child-Pugh classification

   

<0.001

Class A

37 (74 %)

197 (47.9 %)

49 (38.9 %)

Class B

12 (24 %)

169 (41.1 %)

53 (42.1 %)

Class C

1 (2 %)

45 (10.9 %)

24 (19 %)

HVPG (mmHg), Median (Interquartile range)

9.2 (7.2–16.7)

14.6 (10.1–19.3)

17.3 (12.3–21.5)

<0.001

MELD score

6.00 (6.00–8.07)

9.41 (6.00–12.85)

10.64 (6.94–14.73)

<0.001

Albumin (g/dL)

3.7 (3.0–4.1)

3.3 (2.8–3.8)

3.2 (2.8–3.6)

0.001

Total bilirubin (mg/dL)

0.9 (0.6–1.2)

1.4 (0.8–2.5)

1.9 (1.0–4.3)

<0.001

Platelet count (x 103/mL)

141.5 (94.8–214.3)

103 (75–156)

104 (66.8–167)

0.004

Prothrombin time (INR)

1.12 (1.04–1.32)

1.26 (1.11–1.44)

1.29 (1.15–1.49)

<0.001

Survival

46 (92 %)

327 (79.6 %)

95 (75.4 %)

 

HCC

5 (10 %)

43 (10.5 %)

6 (4.8 %)

 

HVPG, Severe PHG vs Mild PHG: P = 0.001, Severe PHG vs No PHG: P < 0.001, Mild PHG vs No PHG: P < 0.001

MELD score, Severe PHG vs Mild PHG: P = 0.015, Severe PHG vs No PHG: P < 0.001, Mild PHG vs No PHG: P < 0.001

Albumin, Severe PHG vs Mild PHG: P = 0.18, Severe PHG vs No PHG: P < 0.001, Mild PHG vs No PHG: P = 0.002

Total bilirubin, Severe PHG vs Mild PHG: P < 0.001, Severe PHG vs No PHG: P < 0.001, Mild PHG vs No PHG: P < 0.001

Platelet, Severe PHG vs Mild PHG: P = 0.49, Severe PHG vs No PHG: P = 0.004, Mild PHG vs No PHG: P = 0.001

INR, Severe PHG vs Mild PHG: P = 0.14, Severe PHG vs No PHG: P < 0.001, Mild PHG vs No PHG: P < 0.001

Survival, Severe PHG vs Mild PHG: P = 0.08, Severe PHG vs No PHG: P < 0.001, Mild PHG vs No PHG: P = 0.008

HCC, severe PHG vs Mild PHG: P = 0.63, Severe PHG vs No PHG: P = 0.34, Mild PHG vs No PHG: P = 0.32

N number, HBV hepatitis B virus, HCV hepatitis C virus, PHG portal hypertensive gastropathy, HVPG hepatic vein pressure gradient, MELD model for end-stage liver disease, INR international normalized ratio, SD standard deviation, HCC hepatocellular carcinoma

In the analysis of survival, patients without PHG showed a higher survival rate than patients with PHG (92 % vs 78.6 %, 95.33 ± 3.78 vs 74.53 ± 2.21 months, P = 0.004) (Table 2 and Fig. 2a). This finding was also consistent with the analysis stratified by the severity of PHG (severe PHG vs mild PHG, P = 0.008; severe PHG vs no PHG, P < 0.001; mild PHG vs no PHG, P = 0.008) (Table 3, Fig. 2b). The detailed survival months and survival rates are reported in Table 4.
Fig. 2

Survival curve according to the presence of PHG (a) and PHG grade (b). PHG, portal hypertensive gastropathy

Table 4

Survival rate according to the PHG grade

PHG grade

Mean survival (months), Mean ± SD

Survival rate

Overall mortality (%)

1 year (%)

3 years (%)

7 years (%)

No PHG

95.33 ± 3.78

100

88.6

88.6

8

Overall PHG

74.53 ± 2.21

89.9

75.5

54.9

21.4

Mild PHG

76.68 ± 2.40

92.8

78.5

56.4

20.4

Severe PHG

55.48 ± 2.05

79.7

64.3

53.8 (5 years)

24.6

N number, PHG portal hypertensive gastropathy, SD standard deviation

For the development of HCC, there was no significant difference between patients with or without PHG (9.1 % vs 10 %, P = 0.33) (Table 2). This finding was also consistent with the analysis stratified by the severity of PHG (severe PHG vs mild PHG: P = 0.63; severe PHG vs no PHG: P = 0.34; mild PHG vs no PHG: P = 0.32) (Table 3).

The distribution of sex and etiology of LC was different between patients with PHG and without PHG. However, the survival rate was not different between men and women (P = 0.44, log-rank test). In terms of the etiology of LC, the survival rate was only different between patients with CHB-associated LC and those with alcoholic LC (P = 0.03) (Fig. 3). The development of HCC was not significantly different between men and women (P = 0.66, log-rank test). In terms of the etiology of LC, the survival rate was not also different according to the etiology (Additional file 1: Figure S1).
Fig. 3

Survival curve according to the etiology of LC. LC, liver cirrhosis; HBV, hepatitis B virus; HCV, hepatitis C virus

Multivariate analysis for the prediction of survival in patients with LC

In the multivariate analysis of independent risk factors for survival, PHG (severe PHG vs no PHG, HR: 3.29, 95 % CI: 1.12–9.63, P = 0.03) and Child-Pugh classification (Child C vs A, HR: 3.53, 95 % CI: 1.79–6.97, P < 0.001) (Child B vs A, HR: 2.15, 95 % CI: 1.35–3.44, P = 0.001) showed statistically significant associations with survival in patients with LC. Age (HR 1.03, 95 % CI: 1.01–1.06, P = 0.001) and HVPG (HR 1.06, 95 % CI: 1.03–1.08, P < 0.001) showed marginal statistical significance (Table 5). This analysis was controlled for age, sex, etiology of LC, and MELD score.
Table 5

Multivariable analysis for the prediction of survival in patients with LC

Variables, n (%)

HR (95 % CI)

P value

PHG

3.29 (1.12–9.63) (Severe PHG vs No PHG)

P = 0.03

Age

1.03 (1.01–1.06)

P = 0.001

Child-Pugh classification

3.53 (1.79–6.97) (Child C vs A)

P < 0.001

2.15 (1.35–3.44) (Child B vs A)

P = 0.001

HVPG

1.06 (1.03–1.08)

P < 0.001

Controlled for age, sex, etiology, and MELD score

N number, HVPG hepatic vein pressure gradient, PUD peptic ulcer disease, NSAIDs non-steroid anti-inflammatory drugs, LC liver cirrhosis, OR Odds ratio

Discussion

Blood flow congestion secondary to portal hypertension is considered the primary cause of PHG [17]. Imbalances between mucosal protective mechanisms and injury factors resulting from mucosal hemodynamic alterations are believed to induce PHG [18]. Although portal hypertension is the prerequisite for the development of PHG, various other factors, such as inflammatory response, local vascular tone, hepatic function, gastric mucosal perfusion, endotoxin, and gastric sucrose permeability, are suspected to influence the development of PHG [19–22]. Reversible mucosal changes in the stomach have suggested that PHG is a dynamic condition [23, 24]. Several studies have evaluated the correlation of PHG with the severity of liver disease or portal hypertension [5–13]. However, most of these studies have included small populations, and the association remains unclear. Our study included the largest population (n = 587) and evaluated the association of PHG with the development of HCC, as well as with portal hypertension and survival.

PHG was detected in 91.5 % of the total population in our study. This result was consistent with several previous studies (90.1 % in the study by Kim et al. and 93.4 % in the study by Curvêlo et al.) [7, 8]. The reported prevalence of PHG has shown great variation (7–98 %) [25, 26]. Selection bias in the studies, inconsistent endoscopic diagnosis criteria, and the lack of interobserver reliability are suspected causes of variation [27]. A recent study of the reliability of endoscopic diagnosis in PHG showed unsatisfactory results regarding the currently available diagnostic criteria (Baveno, McCormack, and NIEC classification) [27]. Binary criteria, such as the presence or absence of a mosaic-like pattern, red-point lesions and cherry-red spots, showed high inter-observer agreement and high specificity [27]. To minimize bias, our study adopted an analysis of group created according to the presence of PHG or not (binary criteria), in addition to the Baveno III scoring system for PHG, and six experienced endoscopists made decisions by consensus.

In the analysis of the correlation between PHG and the severity of liver disease, PHG showed correlations with Child-Pugh classification, HVPG, and MELD score, as well as laboratory parameters (Table 2). These correlations were also consistent in the analysis according to the severity of PHG (no PHG vs mild PHG vs severe PHG) (Table 3). This finding was consistent with a recent Korean study, which prospectively enrolled 331 patients with LC [8]. Previous studies indicating no definite correlation of PHG with the severity of liver disease have suggested that various factors are associated with the development of PHG [11, 12]. However, reversal or improvement of PHG was observed after treatment with transjugular intrahepatic portosystemic shunt (TIPS), indicating that portal hypertension is the main pathophysiologic mechanism of PHG [24]. These studies cannot definitely explain the cause of reversal of PHG after TIPS. Moreover, only small populations were included in these studies. Large scale studies, including our study, have shown a common association of PHG with the severity of liver disease [8].

Prognostic implications of PHG were also assessed in our study. The survival rates were statistically lower in patients with PHG, and this finding was consistent in the stratified analysis based on the severity of PHG (Tables 2 and 3; Fig. 2). Another large-scale study by Kim et al [8]. also showed consistent results. There was a report indicating an association of HVPG with mortality in patients with decompensated LC [28]. In this study, the cut-off value of HVPG of 18 mm Hg was associated with 2-year mortality in patients with decompensated LC [28]. This value was similar to our data of HVPG in patients with severe PHG (median HVPG 17.3 of mm Hg). Without definite mucosal hemorrhage, incidentally detected PHG is easily neglected by endoscopists. Although this study cannot provide histologic data about the liver, patients with PHG should be considered to have more advanced hepatic disease, associated with a poorer prognosis.

The presence of advanced hepatic fibrosis is related to portal hypertension and the development of HCC. Thus, early detection and treatment of liver fibrosis and its complications are important. After the suggestion of pathophysiologic classification of LC using HVPG by Garcia-Tsao et al. [29], the association of HVPG and the development of HCC have been studied. In a study of patients with decompensated alcoholic LC, the cut-off value for HVPG of 15 mm Hg was associated with the development of HCC [30]. However, in another study of patients with compensated LC, the cut-off value of HVPG 10 mm Hg was associated with the development of HCC [31]. According to our data, the presence of PHG could be used as an index of prognosis. However, the presence of PHG or the degree of PHG was not associated with the development of HCC. As shown in previous studies, many factors are associated with the development of HCC [32]. These factors include viral predisposing conditions, environmental factors, age, sex, genetic susceptibility, and metabolic factors [32]. Considering the risk persisting after sustained virological response in patients with HCV-associated LC or even after HBsAg seroclearance in patients with HBV infection, hemodynamic staging alone cannot predict the development of HCC [33–35].

There were several limitations of our study. This study lacked information about changes in PHG or HVPG according to the treatment of LC. The association of the development of PHG with esophageal or gastric varices could not be assessed because various treatments or even non-treated cases of varices were included in the total population. Despite these limitations, our study included the largest population, and long-term observation was undertaken for the evaluation of prognosis and the development of HCC.

Conclusion

In conclusion, PHG was well correlated with portal hypertension. It could be used as a prognostic factor for LC but not for the prediction of HCC.

Abbreviations

ALT, alanine transaminase; AST, aspartate transaminase; CI, confidence interval; EGD, esophagogastroduodenoscopy; HCC, hepatocellular carcinoma; HCV, hepatitis C virus; HR, hazard ratio; HVPG, hepatic vein pressure gradient; IQR, interquartile ranges; LC, liver cirrhosis; MELD score, The Model for End-stage Liver disease score; n, number; HBV, hepatitis B virus; PHG, portal hypertensive gastropathy

Declarations

Acknowledgements

Not applicable.

Funding

This research was supported by Hallym University Research Fund 2014 (HURF-2014-20).

Availability of data and materials

The dataset supporting the conclusions of this article is (are) included within the article and its additional file.

Authors’ contributions

CSB participated data analysis and interpretation, and article drafting. HSK participated data analysis and interpretation, and article drafting. KTS participated to data analysis and interpretation. SEK participated to data analysis and interpretation. JWP participated to data analysis and interpretation. SHP participated to data analysis and interpretation. HSK participated to data analysis and interpretation. MKJ participated to data analysis and interpretation. SHP participated to data analysis and interpretation. MSL participated to data analysis and interpretation. CKP participated to data analysis and interpretation and revising it critically for important intellectual content. DJK participated to study design, data analysis and interpretation, and gave final approval for publication. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Voluntary participation was encouraged and informed consent to participate in the study was obtained from each patient. Patient records or information was anonymized and de-identified prior to analysis. Consent to publish of each patient data was obtained.

Ethics approval and consent to participate

This study was conducted according to the principles expressed in the Declaration of Helsinki and approved by institutional review board of Chuncheon Sacred Heart hospital before initiating study (2015-120). Voluntary participation was encouraged and informed consent to participate in the study was obtained from each patient. Patient records or information was anonymized and de-identified prior to analysis. Consent to publish of each patient data was obtained.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Internal Medicine, Hallym University College of Medicine, Chuncheon, South Korea
(2)
Department of Internal Medicine, Inje University Haeundae-Paik Hospital, Busan, South Korea

References

  1. de Franchis R. Evolving consensus in portal hypertension. Report of the Baveno IV consensus workshop on methodology of diagnosis and therapy in portal hypertension. J Hepatol. 2005;43(1):167–76.View ArticlePubMedGoogle Scholar
  2. De Palma GD, Rega M, Masone S, Persico F, Siciliano S, Patrone F, Matantuono L, Persico G. Mucosal abnormalities of the small bowel in patients with cirrhosis and portal hypertension: a capsule endoscopy study. Gastrointest Endosc. 2005;62(4):529–34.View ArticlePubMedGoogle Scholar
  3. Westerhoff M, Tretiakova M, Hovan L, Miller J, Noffsinger A, Hart J. CD61, CD31, and CD34 improve diagnostic accuracy in gastric antral vascular ectasia and portal hypertensive gastropathy: An immunohistochemical and digital morphometric study. Am J Surg Pathol. 2010;34(4):494–501.View ArticlePubMedGoogle Scholar
  4. Schepis F, Camma C, Niceforo D, Magnano A, Pallio S, Cinquegrani M, D’amico G, Pasta L, Craxì A, Saitta A, et al. Which patients with cirrhosis should undergo endoscopic screening for esophageal varices detection? Hepatology. 2001;33(2):333–8.View ArticlePubMedGoogle Scholar
  5. Panes J, Bordas JM, Pique JM, Bosch J, García-Pagán JC, Feu F, Casadevall M, Terés J, Rodés J. Increased gastric mucosal perfusion in cirrhotic patients with portal hypertensive gastropathy. Gastroenterology. 1992;103(6):1875–82.View ArticlePubMedGoogle Scholar
  6. Merkel C, Schipilliti M, Bighin R, Bellini B, Angeli P, Bolognesi M, Vescovi F, Gatta A. Portal hypertension and portal hypertensive gastropathy in patients with liver cirrhosis: a haemodynamic study. Dig Liver Dis. 2003;35(4):269–74.View ArticlePubMedGoogle Scholar
  7. Curvelo LA, Brabosa W, Rhor R, Lanzoni V, Parise ER, Ferrari AP, Kondo M. Underlying mechanism of portal hypertensive gastropathy in cirrhosis: a hemodynamic and morphological approach. J Gastroenterol Hepatol. 2009;24(9):1541–6.View ArticlePubMedGoogle Scholar
  8. Kim MY, Choi H, Baik SK, Yea CJ, Won CS, Byun JW, Park SY, Kwon YH, Kim JW, Kim HS, et al. Portal hypertensive gastropathy: correlation with portal hypertension and prognosis in cirrhosis. Dig Dis Sci. 2010;55(12):3561–7.View ArticlePubMedGoogle Scholar
  9. Iwao T, Toyonaga A, Sumino M, Takagi K, Oho K, Nishizono M, Ohkubo K, Inoue R, Sasaki E, Tanikawa K. Portal hypertensive gastropathy in patients with cirrhosis. Gastroenterology. 1992;102(6):2060–5.View ArticlePubMedGoogle Scholar
  10. Ohta M, Hashizume M, Higashi H, Ueno K, Tomikawa M, Kishihara F, Kawanaka H, Tanoue K, Sugimachi K. Portal and gastric mucosal hemodynamics in cirrhotic patients with portal-hypertensive gastropathy. Hepatology. 1994;20(6):1432–6.View ArticlePubMedGoogle Scholar
  11. Bellis L, Nicodemo S, Galossi A, Guarisco R, Spilabotti L, Durola L, Dell’Unto O, Puoti C. Hepatic venous pressure gradient does not correlate with the presence and the severity of portal hypertensive gastropathy in patients with liver cirrhosis. J Gastrointestin Liver Dis. 2007;16(3):273–7.PubMedGoogle Scholar
  12. Quintero E, Pique JM, Bombi JA, Bordas JM, Sentis J, Elena M, Bosch J, Rodes J. Gastric mucosal vascular ectasias causing bleeding in cirrhosis. A distinct entity associated with hypergastrinemia and low serum levels of pepsinogen I. Gastroenterology. 1987;93(5):1054–61.View ArticlePubMedGoogle Scholar
  13. Sarin SK, Sreenivas DV, Lahoti D, Saraya A. Factors influencing development of portal hypertensive gastropathy in patients with portal hypertension. Gastroenterology. 1992;102(3):994–9.View ArticlePubMedGoogle Scholar
  14. Becker U, Deis A, Sorensen TI, Grønbaek M, Borch-Johnsen K, Müller CF, Schnohr P, Jensen G. Prediction of risk of liver disease by alcohol intake, sex, and age: a prospective population study. Hepatology. 1996;23(5):1025–9.View ArticlePubMedGoogle Scholar
  15. McQuade WH, Levy SM, Yanek LR, Davis SW, Liepman MR. Detecting symptoms of alcohol abuse in primary care settings. Arch Fam Med. 2000;9(9):814–21.View ArticlePubMedGoogle Scholar
  16. de Franchis R. Updating consensus in portal hypertension: report of the Baveno III Consensus Workshop on definitions, methodology and therapeutic strategies in portal hypertension. J Hepatol. 2000;33(5):846–52.View ArticlePubMedGoogle Scholar
  17. Ripoll C, Garcia-Tsao G. Management of gastropathy and gastric vascular ectasia in portal hypertension. Clin Liver Dis. 2010;14(2):281–95.View ArticlePubMedPubMed CentralGoogle Scholar
  18. Perini RF, Camara PR, Ferraz JG. Pathogenesis of portal hypertensive gastropathy: translating basic research into clinical practice. Nat Clin Pract Gastroenterol Hepatol. 2009;6(3):150–8.View ArticlePubMedGoogle Scholar
  19. Abbasi A, Bhutto AR, Butt N, Munir SM, Dhillo AK. Frequency of portal hypertensive gastropathy and its relationship with biochemical, haematological and endoscopic features in cirrhosis. J Coll Physicians Surg Pak. 2011;21(12):723–6.PubMedGoogle Scholar
  20. Giofre MR, Meduri G, Pallio S, Calandra S, Magnano A, Niceforo D, Cinquegrani M, di Leo V, Mazzon E, Sturniolo GC, et al. Gastric permeability to sucrose is increased in portal hypertensive gastropathy. Eur J Gastroenterol Hepatol. 2000;12(5):529–33.View ArticlePubMedGoogle Scholar
  21. Panes J, Bordas JM, Pique JM, García-Pagán JC, Feu F, Terés J, Bosch J, Rodés J. Effects of propranolol on gastric mucosal perfusion in cirrhotic patients with portal hypertensive gastropathy. Hepatology. 1993;17(2):213–8.PubMedGoogle Scholar
  22. Lan C, Sun X, Dong L, Huang B, Yuan S, Wu K. The role of endotoxin in the pathogenesis of gastric mucosal damage in cirrhotic rats with portal hypertensive gastropathy. Asian Pac J Trop Med. 2011;4(3):212–4.View ArticlePubMedGoogle Scholar
  23. Primignani M, Carpinelli L, Preatoni P, Battaglia G, Carta A, Prada A, Cestari R, Angeli P, Gatta A, Rossi A, et al. Natural history of portal hypertensive gastropathy in patients with liver cirrhosis. The New Italian Endoscopic Club for the study and treatment of esophageal varices (NIEC). Gastroenterology. 2000;119(1):181–7.View ArticlePubMedGoogle Scholar
  24. Kamath PS, Lacerda M, Ahlquist DA, McKusick MA, Andrews JC, Nagorney DA. Gastric mucosal responses to intrahepatic portosystemic shunting in patients with cirrhosis. Gastroenterology. 2000;118(5):905–11.View ArticlePubMedGoogle Scholar
  25. McCormack TT, Sims J, Eyre-Brook I, Kennedy H, Goepel J, Johnson AG, Triger DR. Gastric lesions in portal hypertension: inflammatory gastritis or congestive gastropathy? Gut. 1985;26(11):1226–32.View ArticlePubMedPubMed CentralGoogle Scholar
  26. Vigneri S, Termini R, Piraino A, Scialabba A, Pisciotta G, Fontana N. The stomach in liver cirrhosis. Endoscopic, morphological, and clinical correlations. Gastroenterology. 1991;101(2):472–8.View ArticlePubMedGoogle Scholar
  27. de Macedo GF, Ferreira FG, Ribeiro MA, Szutan LA, Assef MS, Rossini LG. Reliability in endoscopic diagnosis of portal hypertensive gastropathy. World J Gastrointest Endosc. 2013;5(7):323–31.View ArticlePubMedPubMed CentralGoogle Scholar
  28. Suk KT, Kim CH, Park SH, Sung HT, Choi JY, Han KH, Hong SH, Kim DY, Yoon JH, Kim YS, et al. Comparison of hepatic venous pressure gradient and two models of end-stage liver disease for predicting the survival in patients with decompensated liver cirrhosis. J Clin Gastroenterol. 2012;46(10):880–6.View ArticlePubMedGoogle Scholar
  29. Garcia-Tsao G, Friedman S, Iredale J, Pinzani M. Now there are many (stages) where before there was one: In search of a pathophysiological classification of cirrhosis. Hepatology. 2010;51(4):1445–9.View ArticlePubMedPubMed CentralGoogle Scholar
  30. Kim MY, Baik SK, Yea CJ, Lee IY, Kim HJ, Park KW, Kim HK, Suk KT, Kim JW, Kim HS, et al. Hepatic venous pressure gradient can predict the development of hepatocellular carcinoma and hyponatremia in decompensated alcoholic cirrhosis. Eur J Gastroenterol Hepatol. 2009;21(11):1241–6.View ArticlePubMedGoogle Scholar
  31. Ripoll C, Groszmann RJ, Garcia-Tsao G, Bosch J, Grace N, Burroughs A, Planas R, Escorsell A, Garcia-Pagan JC, Makuch R, et al. Hepatic venous pressure gradient predicts development of hepatocellular carcinoma independently of severity of cirrhosis. J Hepatol. 2009;50(5):923–8.View ArticlePubMedPubMed CentralGoogle Scholar
  32. Herbst DA, Reddy KR. Risk factors for hepatocellular carcinoma. Clinical Liver Disease. 2012;1(6):180–2.View ArticleGoogle Scholar
  33. Pinzone MR, Zanghi AM, Rapisarda L, D’Agata V, Benanti F, Spartà D, Nunnari G, Cacopardo B. Cirrhotic patients are still at risk of developing hepatocellular carcinoma despite Interferon-induced sustained virological response. Eur Rev Med Pharmacol Sci. 2014;18(2 Suppl):11–5.PubMedGoogle Scholar
  34. Aleman S, Rahbin N, Weiland O, Davidsdottir L, Hedenstierna M, Rose N, Verbaan H, Stål P, Carlsson T, Norrgren H, et al. A risk for hepatocellular carcinoma persists long-term after sustained virologic response in patients with hepatitis C-associated liver cirrhosis. Clin Infect Dis. 2013;57(2):230–6.View ArticlePubMedGoogle Scholar
  35. Simonetti J, Bulkow L, McMahon BJ, Homan C, Snowball M, Negus S, Williams J, Livingston SE. Clearance of hepatitis B surface antigen and risk of hepatocellular carcinoma in a cohort chronically infected with hepatitis B virus. Hepatology. 2010;51(5):1531–7.View ArticlePubMedGoogle Scholar

Copyright

© The Author(s). 2016

Advertisement

BMC Gastroenterology

ISSN: 1471-230X

Contact us