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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 4  |  Issue : 3  |  Page : 332-338

Assessment of portal hypertensive enteropathy in patients with liver cirrhosis


1 Department of Pathology, Al-Azhar University, Cairo, Egypt
2 Pathology, Al-Azhar University, Cairo, Egypt
3 Department of Tropical Medicine, Al-Azhar University, Cairo, Egypt

Date of Submission01-Feb-2020
Date of Decision26-Mar-2020
Date of Acceptance30-Mar-2020
Date of Web Publication2-Oct-2020

Correspondence Address:
MD Waleed M Mousa
Tropical Medicine, Al-Azhar University, Gouhar AL-Kaed Street, El-Hussein University Hospital, Al-Azhar University, Al-Darasah, Cairo, 11675
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/sjamf.sjamf_13_20

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  Abstract 


Background Portal hypertensive enteropathy remains difficult to diagnose in patients with cirrhosis and portal hypertension (PHT). Limited test choices exist for the inspection of the small bowel in these patients. Small-bowel endoscopy like double-balloon enteroscopy (DBE) is ideal in this situation but rarely performed. We aimed to determine the prevalence of portal hypertensive enteropathy using DBE in the patient population with PHT and correlate its presence with clinical, radiological, and histological findings.
Patients and methods Thirty-two patients with PHT were included along with 10 controls without the criteria of PHT. All patients and control groups underwent blood tests, ultrasonography, gastroscopy, and enteroscopy. The small-bowel findings by DBE were categorized as inflammatory-like and vascular lesions. The small-bowel changes either endoscopically or histologically were analyzed to find out any association with various demographic, clinical, ultrasonographic, and endoscopic variables.
Results The frequency of portal enteropathy in our study was 65.6% (21 patients out of 32) and it had positive correlation with the presence of esophageal varices, PHG, and Child-Pugh score. We found that there is statistically significant difference between the results of histology among patients and control groups not only in the jejunal specimen but also in the gastric and duodenal ones. The correlation with the endoscopic picture was statistically not significant.
Conclusion Small-bowel mucosal and vascular changes related to PHT were seen in a significantly higher number of patients with cirrhosis and PHT.

Keywords: cirrhosis, double-balloon enteroscopy, portal hypertensive enteropathy


How to cite this article:
Afifi MA, Hamid GA, Mousa WM, Ghareb M. Assessment of portal hypertensive enteropathy in patients with liver cirrhosis. Sci J Al-Azhar Med Fac Girls 2020;4:332-8

How to cite this URL:
Afifi MA, Hamid GA, Mousa WM, Ghareb M. Assessment of portal hypertensive enteropathy in patients with liver cirrhosis. Sci J Al-Azhar Med Fac Girls [serial online] 2020 [cited 2020 Oct 31];4:332-8. Available from: http://www.sjamf.eg.net/text.asp?2020/4/3/332/296921




  Introduction Top


In 1902, Gilbert and Carnot introduced the term portal hypertension (PHT) to describe a condition characterized by splenomegaly, ascites, and gastrointestinal bleeding [1]. In the gastrointestinal tract specifically, there are many pathological changes attributed to PHT. The most well-recognized are esophageal or gastric and rectal varices, and portal hypertensive gastropathy (PHG). Small-bowel capsule endoscopy and double-balloon enteroscopy have enabled us to explore subtle findings in the small bowel in great detail [2],[3]. Over the last few years, it has emerged that portal hypertensive enteropathy (PHE) is a common complication of PHT. First described by De Palma et al. [4], it should now be considered well defined. The term PHE encompasses the spectrum of mucosal abnormalities noted in the small intestine in patients with PHT [5]. Both brisk and indolent bleeding are known to occur from such mucosal lesions. Although various diagnostic modalities like small-bowel follow-through, ileocolonoscopy, capsule endoscopy, push enteroscopy, or deep enteroscopy have been used to identify the prevalence of PHE; the diagnostic and therapeutic yield of enteroscopy is much higher in identifying such lesions [6].


  Aim Top


In this study, we aimed to determine the endoscopic and histologic changes of the small intestine in PHT to determine the prevalence, the diagnostic criteria, and the clinical impact of PHE as well as any possible intercorrelation between the endoscopic and histologic picture of the gastric, duodenal, and jejunal mucosa.


  Patients and methods Top


This study was conducted prospectively on 32 cirrhotic patients with evidence of PHT and 10 controls without the criteria of PHT. The patients were selected from all patients admitted to the Tropical Medicine Department, Al-Azhar University Hospitals in the period from January to December 2016, known to have liver cirrhosis and clinically significant PHT. Patients with severe renal or cardiac impairment occlusion (confirmed by color Doppler sonography), previous history of chronic small-bowel disease, for example: Crohn’s disease or history of recent or current intake of NSAIDs or vasoactive drugs such as beta blockers or nitrates that can affect the degree of PHT or intestinal mucosa were excluded from the study.

After getting an informed consent the following demographic, clinical, laboratory, radiological, endoscopic, and histological characteristics were recorded: age, sex, etiology of PHT, and previous history of upper gastrointestinal bleeding and any endoscopic intervention. The laboratory parameters including complete blood count, liver function tests, and prothrombin time and renal function tests were recorded to calculate the Child-Pugh-Turcotte score. Abdominal ultrasonography was done with special concern on criteria suggestive of liver cirrhosis and PHT. Subsequently, double-balloon enteroscopy was performed. Presence of esophageal varices, gastric varices, portal hypertensive gastropathy, and duodenopathy were noted during esophagogastrodeudenoscopy (EGD). Esophageal varices were graded according to Westby classification [7]. Portal hypertensive gastropathy was graded according to McCormack [10]. PHE changes were graded according to De Palma et al. [4], which included mucosal inflammatory-like abnormalities (fold thickening, edema, erythema, granularity, friability) and vascular lesions (cherry red spots, telangiectasias, or angiodysplasia-like lesions, and varices).

Histopathological examination

Three pinch biopsies were taken from each of the jejunum (as far as possible), the second duodenal segment and the fundus of the stomach.

Each section was examined for congestion, vasodilatation (ectasia), edema of the lamina propria, and inflammatory cellular infiltration.

Control individuals were subjected to abdominal sonography and enteroscopy including upper endoscopy as well as jejunal, duodenal, and fundal biopsies.

Correlations

Histological findings of the patient group were compared with the control group. The intercorrelation between the stomach, duodenum, and the jejunum, both endoscopically and histologically as well as the correlation between endoscopic, histologic, and radiologic findings were assessed.

Ethical aspect

Approving protocol

The current protocol is approved by the Committee of Tropical Medicine Department and by the Committee of Faculty of Medicine Al-Azhar University.

Patients consent

All patients that were included in the current study signed an approved consent from Al-Azhar University Ethics Committee.

Statistical analysis

All patient data were tabulated and processed using the statistics program ‘SPSS’ [9] for Microsoft Windows (SPSS version 23 belong To IBM corporation situated in Armonk, New York, USA).

Quantitative variables were expressed by mean and SD. Student’s t test and analysis of variance tests were used when appropriate.

Fisher’s exact test was used to compare qualitative variables.

P value was considered significant if less than 0.05 and highly significant when less than 0.001.


  Results Top


This study was conducted on 32 patients with liver cirrhosis and PHT, who fulfilled the inclusion criteria during the study period. The control group consisted of 10 individuals without the criteria of PHT. The patients were 20 (60%) men and 12 (40%) women with an age range from 30 to 61 years with a mean±SD of 47.30±7.69 years ([Table 1],[Table 2],[Table 3],[Table 4]).
Table 1 Clinical features of the patient groups

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Table 2 Laboratory features of the patient groups

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Table 3 Ultrasonographic findings of the patients group

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Table 4 Cause of cirrhosis and modified Child-Pugh score are shown in [Table 3]

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Endoscopic findings

All patients included in our study had esophageal varices distributed as follows: three (9.3%) were eradicated, eight (25%) patients had grade I, eight (25%) patients had grade II, six (18.75%) patients had grade III, and seven patients had grade IV esophageal varices. In addition, 28 patients had PHG ranging from mild, moderate to severe. As regards enteroscopic findings, PHE (duodenopathy or jejunopathy) was suggested if the following descriptive criteria are present: thickening of folds causing narrowing of the interfold spaces, patchy and/or diffuse mucosal hyperemia, presence of petechiae (fine red spots) on top, presence of angioectasia; and so, the frequency of enteropathy in the jejunum according to the suggested descriptive criteria was 65.6% (21 patients out of 32).

The presence of PHE was strongly associated with Child-Pugh score; history of gastrointestinal bleeding or intervention for such bleeding; size of esophageal varices, and presence of PHG. Concerning histology, four parameters were assessed in each specimen, namely the congestion, ectasia of mucosal vessels, cellular infiltration, and edema of the lamina propria (Tables 5 and 6).
Table 6 Histological finding of the studied groups; patients versus control (jejunal sample)

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We found that there is statistically significant difference between the results of histology among patients and control groups not only in the jejunal specimen but also in the gastric and duodenal ones. The correlation with the endoscopic picture was statistically not significant ([Figure 1],[Figure 2],[Figure 3],[Figure 4],[Figure 5],[Figure 6],[Inline 1], [Figure 7],[Figure 8],[Figure 9],[Figure 10]).
Figure 1 Normal jejunum.

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Figure 2 Normal interfold spaces.

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Figure 3 Marked thickening and edema of the jejunum.

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Figure 4 Submucosal petechiae.

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Figure 5 Marked edema and thickening.

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Figure 6 Marked edema and thickening.

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Figure 7 Normal jejunal mucosa (hematoxylin and eosin).

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Figure 8 Jejunal mucosa showing edema, congestion, and inflammatory reaction.

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Figure 9 Jejunal mucosa showing marked edema, congestion, and inflammatory reaction, ectatic congested submucosal vessel.

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Figure 10 Jejunal mucosa showing marked edema, increased vascularity, mild dilatation, and congestion. Marked edema of the submucosa is noted.

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  Discussion Top


Portal hypertension can be a cause of life-threatening bleeding, mainly from esophageal varices and/or gastric varices. PHG and colopathy are also well-characterized manifestations of PH. The advent of capsule endoscopy and different types of enteroscopy a few years back enabled us to first describe and then characterize PHE. Further data on PHE have recently been produced but the true prevalence and associated clinical factors remain unclear. The aim of this prospective study was to define PHE by detecting endoscopic and histologic changes of the small intestine in PHT, to assess its clinical impact and to correlate this newly defined entity with the etiology of the liver disease, liver dysfunction grade, and the presence of collaterals.

Furthermore, this study aimed to find the endoscopic and histologic intercorrelationship between the PHE and the well-studied portal hypertensive gastropathy.

The number of patients included in this study was sufficient to perform statistical analysis and it included 32 patients and 10 controls, combining enteroscopy, histological examination of the small intestine in PHT, besides ultrasonography in addition to complete clinical and laboratory workup.

Concerning endoscopy, PHG was diagnosed and graded according to McCormack [8]. We chose the fundus as a site of tissue sampling as it is according to McCormack [8],[10] the most common site affected by congestive changes in PHT. The antrum, besides being less commonly affected, represents the site of two common different pathologies that can affect the endoscopic and histologic appearances, namely the gastric antral vascular ectasia and Helicobacter pylori-associated antral gastritis. Endoscopic examination of the patients group showed absence of esophageal varices in three patients because of therapeutic eradication.

Portal hypertensive gastropathy was found in 87.5% of patients. This relatively high incidence in our patients lies in the high side of the wide range reported in the literature (98%) [8],[9],[11]. Viggiano and Gostout [5] explained this variable frequency by the differences in ethnic groups examined, observer variability, or differences in endoscopic techniques.

Portal hypertensive gastropathy was correlated with the presence of esophageal varices and history of sclerotherapy or band ligation similar to the majority of the studies published in this field [8],[9],[12],[13]. The mechanism by which sclerotherapy could increase the risk of congestive gastropathy remains unclear, but gastric mucosal congestion caused by reduction of the collateral blood flow through varices by sclerotherapy was the advocated theory [8],[9].

The prevalence of PHE in our study was 65.6%, which is in accordance with many previous studies [3],[4],[6]. It is important to stress that Child-Pugh score, which is a good predictor of liver disease staging, was significantly correlated with the presence of PHE. We would argue then that PHE is commoner in patients with more pronounced PHT as manifested by the presence of esophageal varices, gastric varices, and PHG and is in accordance with observations by Takahashi et al. [14] and Aoyama et al. [15], who showed a correlation between PHE and hepatic portal venous gradient (HPVG). Concerning histology, four parameters were assessed in each specimen, namely the congestion and the ectasia of mucosal vessels and cellular infiltration and edema of the lamina propria. In spite of a normal endoscopic appearance, the controls showed mild histological changes in 35–100% of the cases and sometimes (in 0–15%) marked changes were also seen. Compared with patients who showed much more important frequencies of marked histological changes (up to 56%) and nearly no negative findings (<2%), the difference was statistically highly significant for each separate parameter. We may assume that the histology of an endoscopically normal digestive mucosa in nonportal hypertensive Egyptian individuals may show mild histologic changes caused probably by immunological factors (infectious, chemical, allergic, etc.). This finding is in agreement with a rather old but pioneer study performed in 1969 by Halsted et al. [16] from USA and Sheir from Egypt. Marked changes occurred in patients’ small bowel (duodenum and jejunum) in frequencies between 13 and 27% with the following order of decreasing frequency (ectasia, edema, infiltration, and congestion).The correlation with the endoscopic picture was statistically not significant. The lack of a positive correlation between endoscopy and histology was nearly constant in the published comparative studies [17], while Misra et al. [18] reported that ‘histological’ gastropathy is more frequent than ‘endoscopic’ gastropathy; Lastly, this work can be considered as a preliminary study involving many variables and new intercorrelations. Results may not be all conclusive and conclusions may not be all directly applicable clinically. However, the guidance to a step forward was hopefully given and a new field was open for more comprehensive and better targeted future studies.


  Conclusion Top


Small-bowel mucosal and vascular changes related to PHT were seen in significantly higher number of patients with cirrhosis with PHT than in cirrhotics without PHT.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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6.
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Primignani M, Carpinelli L, Preatoni P, Battagalia G, Carta A, Prada A et al. Natural history of portal hypertensive gastropathy with liver cirrhosis. Gastroenterology 2000; 119:181.  Back to cited text no. 13
    
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Takahashi Y, Fujimori S, Narahara Y, Gudis K, Ensaka Y, Kosugi Y et al. Small intestinal edema has the strongest correlation with portal venous pressure amongst capsule endoscopy findings. Digestion 2012; 85:48–54.  Back to cited text no. 14
    
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Aoyama T, Oka S, Aikata H, Igawa A, Nakano M, Naeshiro N et al. Major predictors of portal hypertensive enteropathy in patients with liver cirrhosis. J Gastroenterol Hepatol 2015; 30:124–130.  Back to cited text no. 15
    
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Halsted CH, Sheir S, Sourial N, Patwardhan VN. Small intestinal structure and absorption in Egypt. Am J Clin Nutr 1969; 22:744–754.  Back to cited text no. 16
    
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Misra SP, Dwivedi M, Misra V, Agarwal SK, Gupta R, Gupta SC, Mital VP. Endoscopic and histologic appearance of gastric mucosa in patients with portal hypertension. Gastrointest Endosc 1990; 36:575.  Back to cited text no. 18
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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Abstract
Introduction
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Patients and methods
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