Mucosal Changes in Portal Hypertension

Fouad I. Thakeb , Ayman A.Yosry , Iman M.Hamza

Endemic Medical Department , Hepato- Gastroenterology Division , Cairo
University ,Egypt

Abstract

The gut mucosa in portal hypertension is the seat of microcirculatory changes that
compromise its integrity and increase its susceptibility to damage. There is mucosal
and submucosal angiogenesis, vascular ectasia and dilation with little associated
inflammatory activity. The changes in the stomach (portal hypertensive gastropathy)
have been the most studied and can be a common source of bleeding. Small bowel
involvement (portal hypertensive enteropathy) is usually asymptomatic but may be a
source of occult blood loss. Colon involvement (portal hypertensive colopathy) has
been associated with bleeding and may mimic inflammatory bowel disease. The
mucosal changes in portalo hypertension may require pharmacological, directed
endoscopic, or portal decompressive therapy . Transjugular intrahepatic
portosystemic shunt ( TIPS) has recently been suggested to be useful in patients
unresponsive to other modalities . The recently observed physiologic alterations,
diagnostic modalities and treatment options will be reviewed in this article.

Key Words

Portal Hypertension, portal hypertensive gastropathy, jejunopathy, Gastric

Vascular Ectasia ,varices

Most clinicians would agree that the pathophysiological mechanisms of varices are
interrelated with the mucosal changes of portal hypertension(PH). The topic of
varices (esophageal, gastric, or ectopic ) is well studied 1, however ,the mucosal
changes in the context of PH needs further elaboration. In addition ,such changes
frequently encountered during endoscopy and may present by gastrointestinal (GI)
bleeding and or GI disturbance of clinical relevance .

This review will cover the mucosal changes of the stomach , small intestine ,
rectum and colon avoiding varices for precision.
Portal hypertensive gastropathy(PHG):
The hallmarks of the lesions in PHG are ectatic vessels in the mucosa and
submucosa with insignificant inflammatory cellular infiltrate 2,3. Its prevalence
among portal hypertensive patients ranges from 7% to 41% 4. In the largest study on
the natural history of PHG , the overall prevalence of this condition in patients with
cirrhosis was 80 % 5.
The mechanisms involved in the pathogenesis of PHG have not been fully
elucidated, yet chronic increase in the portal pressure is a prerequisite for its
development 2,3. Several factors, with varying degrees of involvement, are
implicated in the mechanism of PHG e.g. neurohumoral or paracrine substances,

1
hypervolemia, meals, tissue hypoxia and in certain cases hepatocelluar insufficiency
6.
The gastric mucosal blood flow state is debatable . Decrease in blood flow to
the mucosa and increased blood flow to the submucosa, muscle, and serosal layers
have been documented in PHG 7,8. Moreover , a higher hemokinetic stress in severe
PHG cases than in mild cases or controls is proved by using endoscopic laser Doppler
flowmetry 9.
Many trials have evaluated the portal hypertensive mucosa in relation to many
internal and external factors ,it is worth to mention the damaging effects proved
by the decreased gastric mucosal prostaglandin E2 generation in PHG 10. The
increased expression of TNF-α in animal models of PHG causes more mucosal
damage. 11. Up to date , there is no evidence that the presence or the severity of
PHG is dependent on the presence of H-pylori 12,13,14. Sarin et al. has confirmed
that PHG is greatly influenced by the severity of liver disease. Conversely,
Primignani et al. suggests that the correlation is weak 15,5.

Studying the impact of variceal eradication by sclerotherapy or ligation (EVS

or EVL) on PHG revealed the whole spectrum of probabilities . Sarin et al. reported
that EVS is incriminated in worsening PHG as compared to EVL. Although patients
in this study were of a variable spectrum of liver disease (cirrhosis, fibrosis, extra-
hepatic portal vein obstruction and Budd-Chiari cases), yet it had the most prolonged
duration of follow up (23.2 +/- 3.4 months) .Other studies have flipped the coin,
incriminating EVL as compared to EVS 16,17. While Hou et al. Didn't find any
significant difference between either of EVL and EVS on PHG 18.
.
The identification of endoscopic lesions of PHG allowed the development of
a reproducible classification defining mild and severe pictures as well as the
conduction of natural history studies 19,20. The elementary lesions in PHG are mosaic
like pattern ,red point lesion, cherry red spots and black brown spots .According to
the New Italian Endoscopic Club, in mild PHG the gastric mucosa often looks
reddened and edematous with a snakeskin or mosaic pattern. Severe PHG is defined
by cherry red spots, which are typically very friable and can actively bleed during
endoscopy. Such changes are typically localised to the fundus or corpus of the
stomach 21.
There is no specific histology nor correlation between the endoscopic and
the histologic features in PHG 22, 23. Ectasia and sclerosis of the wall of the mucosal
capillaries and venules are common findings with venous congestion. Therefore,
Misra et al. has stated that the thick gastric mucosal capillary wall is a reliable
histological marker of portal hypertension than dilated gastric mucosal capillaries 24.

Patients with PHG may present with clinically significant blood loss, melena,
or more commonly chronic anemia 10,11. The incidence of bleeding is more common
as chronic bleeding (12%) than acute bleeding (2.5%). Bleeding related mortality
reaches 12.5% 25,26, 5 . Zoli et al. study has mentioned that patients with severe
PHG who have severe liver dysfunction, are liable to develop future variceal
bleeding 27. Other studies didn't find any correlation of PHG to: (i) history of
upper GI bleed; (ii) size of varices; (iii) etiology of liver cirrhosis; or (iv) liver
function status . The prevalence of PHG was found higher in patients with
esophagogastric varices (74 / 107; 69%) compared to those with esophageal varices

2
alone (68 / 123; 55%; P < 0.05). A recent study by Stewart and Sanyal showed a
stepwise increase in PHG-related bleeding risk with increasing PHG scores 28.
β- blockers (propranolol),somatostatin, octreotide , vasopressin, terlipressin
and estrogen have been proposed for the treatment of PHG based on their ability to
decrease gastric perfusion. 29,30,1. β- blockers are the drug of choice for prevention
of GI bleeding in PHG , with the dosage titrated up to achieve a resting heart rate of
approximately 60 beats per minute. In patients who do not respond to beta-blockers, a
TIPS should be placed.; Portosystemic shunt surgery is another alternative in the
suitable candidate 29,31,32, 33 .
Due to the lack of randomized studies , the fluctuating nature of PHG and
possibly unreported failures, both TIPS and shunt surgery should be considered
only as a rescue therapies for the uncommon patients who has repeated bleeding
from PHG despite propranolol treatment. Liver transplantation reverses portal
hypertension and therefore effectively treats PHG 34,35.

Gastric antral vascular ectasia (GAVE):

GAVE ,also known as watermelon stomach , is relatively rare . It is

characterised by red patches or spots in either a diffuse or linear array in the antrum of
the stomach , which can result in significant blood loss and leads to chronic iron
deficiency anemia that is difficult to treat 36, 37, 21.

Its etiology is unclear. Vasoactive substances may play an important role in

the etiology of vascular ectasia. Neuroendocrine cells containing vasoactive intestinal
peptide and 5-hydroxtryptamine have been found close to the vessels in the lamina
propria of resected specimens from GAVE patients .So, these mediators may be
responsible for the vasodilatation and thus the propensity to bleed .GAVE in cirrhotic
patients may be explained by the shunting of blood and altered metabolism of
vasoactive substances in the presence of liver disease 38,39,40 . Moreover , abnormal
response to mechanical antral stress is another factor 41,42 .

GAVE have several disease association as primary biliary cirrhosis (PBC) ,

connective tissue disease 43,44 ,etc…More than 70% of patients with GAVE
syndrome do not have cirrhosis or portal hypertension (PBC). However, In the setting
of cirrhosis, GAVE syndrome can be difficult to differentiate from PHG. Both
conditions are diagnosed endoscopically as collections of discrete red spots of ectatic
vessels arranged in stripes along the antral rugal folds; however, the red spots of PHG
appear in a background of mucosal mosaic appearance, but the mucosa underlying
GAVE is normal 22. Histologically , vascular ectasia in GAVE are seen in the
mucosa associated with fibrin thrombi ,fibrohylinosis and spindle cell proliferation
45.

Drugs of reported benefit include estrogen and progesterone, in small series of

patients , failure to find benfit from octreotide 46.47.48,49,50 .
The success of endoscopic therapies have been reported to improve lesions
and decrease blood requirements , although , such treatments are not effective in

3
patients with diffuse GAVE , such modalities include cautery by Argon Plasma
Coagulator ,heater probe ,or Yag laser . Surgical treatment, including antrectomy,
can cure GAVE syndrome, but in patients with cirrhosis and portal hypertension ,
the morbidity of surgery may be reduced by reducing portal pressure 51,52,53,54,55.

Gastroduodenal ulcers and gastroduodenal erosions are particularly frequent in

cirrhotic patients, but their precise cause is unclear. However, the postulation that
portal hypertensive mucosa is relatively ischemic and is liable to noxious injury may
as well explain the association of such lesions 56.

Portal Hypertensive Enteropathy(PHE)

Small bowel mucosa in portal hypertension was recently assessed extensively 57,58 .
It is a recognized potential source of bleeding in portal hypertension. However, the
frequency of its involvement is unknown. 57. Nagral et al. has claimed that PHE
is part of the spectrum of congestive gastroenteropathy and occurs at least as
frequently as changes in the stomach and duodenum 58. In addition , its incidence
doesn't correlate with the Child-Pugh score or with prior sclerotherapy 59 . Similar
to PHG, several incriminating factors have been proposed including circulating
hormonal vasodilators from intestinal origin such as glucagon, insufficiently cleared
by the liver, as well as increased nitric oxide production. Glucagon in a dose sufficient
to acutely elevate portal venous pressure aggravates noxious injury of the mucosa in
rats with portal hypertension. Infusion of a portal hypotensive dose of somatostatin
reverses these changes 60

Misra et al has reported a significant dilatation in the mucosal vessels with

thickened walls in duodenal and jejunal biopsy specimens in portal hypertensive
patients compared to controls ( 67% and 71% versus 27% and 2% respectively) 57 .
Increased mucosal mast cell infiltration suggests an inflammatory background for
PHE in addition to the documented vascular changes. Other important histologic
features in the portal hypertensive patients include edema of the lamina propria,
fibromuscular proliferation, a decreased villous/crypt ratio, and thickened muscularis
mucosae. The clinical implication of these changes is the increased chance of occult
gastrointestinal blood loss 57. PHE is usually asymptomatic, Massive hemorrhage has
only rarely been described and its management is controversial Gastrointestinal wall
thickening is common on contrast-enhanced abdominal CT scans. It involves
multiple segments( commonly jejunum and ascending colon ) 61 .
Protein loosing enteropathy and intestinal lymphagiectasia in portal
hypertension drew the attention of researchers 62.Stanley et al. recently suggested
that the mucosal congestion may lead to protein loss in addition to blood loss ,
probably by dysfunction of the intestinal lymphatics ,and this could be corrected by
TIPS 63.
Functionally, the spectrum of portal hypertension in the gastrointestinal tract still
extends to include altered intestinal motility with delayed transit, mainly in the
proximal part of the small intestine, which may predispose to bacterial overgrowth
and malabsorption 64,65.

4
 Portal hypertensive colopathy( PHC)
PHC has been reported in cirrhotics 66 , it refers to mucosal edema,
erythema, granularity, friability, and vascular lesions in portal hypertension , findings
that may be confused with colitis 67. Misra et al. reported dilated tortuous
mucosal capillaries with irregular thickening of wall, edema of lamina propria and
mild chronic inflammatory infiltrate as the major histopathological changes seen in
colonic biopsies of patients with PHC 68. The histological changes have no
correlation with the clinical or endoscopic findings, however, the thickness of the
capillary wall is higher in patients who had undergone sclerotherapy .

Many endoscopic abnormalities are mentioned in this setting such as anorectal

and recto-sigmoid varices , hemorrhoids, multiple vascular ectasia like lesions, and
nonspecific inflammatory changes. Such lesions could not be correlated with the
degree of esophageal varices, therapy by EVL or EVS, the risk of variceal bleeding,
presence of PHG or gastric varices ,Child's grading, the etiology of cirrhosis, or the
bleeding risk from the lower gastrointestinal tract 66.

Rectal EUS is used recently for evaluation of the anorectal region in portal
hypertension . Dhiman et al . studied changes in the venous system of the rectum
using endoscopy and EUS in 60 patients with portal hypertension (cirrhotic 41,
noncirrhotic 19) and 10 controls 69. Prevalence of rectal varices was 43.3% on
endoscopy and 75% on EUS (p < 0.0005). Congestive rectopathy was found in
38.3% of patients. Multiple small dilated vessels in the submucosa were seen in
23.3% of patients on rectal EUS. The development of these vascular changes was
significantly influenced by sclerotherapy, but not by higher grade of esophageal
varices, the etiology of portal hypertension, or severity of liver disease.
The mucosal changes in PHC may require pharmacological, directed
endoscopic, or portal decompressive therapy , so octreotide may find a place in its
treatment. TIPS has recently been suggested to be useful in the therapy of bleeding
from parastomal , vascular ectasia like lesions or anorectal varices in patients
unresponsive to conservative therapy. 27,70,,71,72.,73
Rarely reported complications of portal hypertension include Pneumatosis
coli , with little clinical significance except , the significant drop of these changes
post-transplantation and cholangiopathy, which may occur in cases of extrahepatic
portal venous obstruction. Strictures and caliber irregularities have been described in
the biliary tree 74

. The reflection of portal hypertension on intestinal function was assessed in a

study by Taylor and co-workers , where they reported impaired mucosal
absorptive capacity in portal hypertensive patients as reflected by reduced
excretion of each of 3-O-methyl-D-glucose, D-xylose and L-rhamnose in them 75.
Alterations in gastric emptying with portal hypertension has no causative role in
the mucosal changes of PHG 78.

5
Conclusion :
Mucosal lesions in portal hypertension are common. Bleeding from PHG and PHE is
usually chronic manifesting with anemia and transfusion dependency but intermittent
overt bleeding can occur, most often in the form of melena. Patients with PHC may
have occult blood loss or overt hematochezia. These mucosal lesions are generally
diagnosed endoscopically but histological confirmation is needed when other similar
conditions such as GAVE, H. pylori infection or undefined colonic lesions are
suspected. Reduction of the portal pressure is the mainstay of treatment. Beta-
blockers are the drug of choice for treatment, and TIPS should be considered for
patients who do not respond to beta-blockers. Liver transplantation reverses portal
hypertension and therefore treats the portal hypertensive gastroenteropathy.

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