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Liver involvement in celiac disease
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     Department of Reproductive Medicine and Child Development University of Pisa, Gastroenterology and Liver Unit and IsMeTT, University of Pittsburgh Medical Center, Palermo, Italy

    Abstract

    Celiac disease may present as a cryptogenic liver disorder being found in 5-10 % of patients with a persistent and cryptogenetic elevation of serum aminotransferase activity. In fact, a wide spectrum of liver injuries in children and adults may be related to CD and in particular: (1) a mild parenchymal damage characterised by absence of any clinical sign or symptom suggesting a chronic liver disease and by non-specific histological changes reversible on a gluten-free diet; (2) a chronic inflammatory liver injury of autoimmune mechanism, including autoimmune hepatitis, primary sclerosing cholangitis and primary biliary cirrhosis, that may lead to fibrosis and cirrhosis, generally unaffected by gluten withdrawal and necessitating an immunosuppressive treatment; (3) a severe liver failure potentially treatable by a gluten-free diet. Such different types of liver injuries may represent a spectrum of a same disorder where individual factors, such as genetic predisposition, precocity and duration of exposure to gluten may influence the reversibility of liver damage. A rigorous cross-checking for a asymptomatic liver damage in CD individuals and conversely, for CD in any cryptogenic liver disorder including end-stage liver failure is recommended.

    Keywords: Celiac disease; Autoimmune liver disease; Acute liver failure; Cryptogenic liver damage

    A possible liver involvement in patients with celiac disease (CD) was first described in 1977.[1] Even if, due to the high prevalence of CD in the general population, a fortuitous association between any type of liver lesion and CD could not be excluded, however, nowadays, there is growing evidence that a wide spectrum of liver injuries in children and adults may be related to CD [Table 2][2] and in particular:

    a mild type of parenchimal damage reversible on a gluten-free diet;

    a chronic inflammatory liver injury that may lead to fibrosis and cirrhosis, generally unaffected by gluten withdrawal;

    a severe liver failure potentially treatable by a gluten-free diet.

    More rarely, other types of liver lesions including fatty liver[3] nodular regenerative hyperplasia[4] and hepatocellular carcinoma, may occur.[1]

    Persistent elevation of serum aminotransferase activity is the most common liver abnormality found in untreated CD.[2] Hagander first in 1977 found that almost 40% of 74 untreated coeliac adult patients showed, at diagnosis, an hypertransaminasemia, in most cases reversible with a gluten free diet (GFD).[5] An histological evaluation, available in 13 patients, demonstrated a mild reactive hepatitis in 5, and different types of liver lesion ranging from liver steatosis to pronounced fibrosis and cirrhosis in the 7 other patients.[5] It was later shown that, also in young children with CD and gastrointestinal symptoms, mild to moderate elevation of serum aminotransferase activity, usually resolving with a GFD, may occur, at diagnosis, in up to 60% of cases.[6] Liver histology showed, in this case, a preserved liver architecture with a mild mononuclear infiltrate of the portal tract and a slight hyperplasia of the Kupffer cells.[7] On the other hand, celiac disease may present as a cryptogenic liver disorder. Such an onset was first described in 1986, in a young girl with persistent and cryptogenic elevation of serum aminotransferase and a mild reactive hepatitis. In this case the diagnosis of CD was suggested by an high titre of antireticulin antibody, serendipitously found on autoantibody screening.[8] This was later confirmed in a series of 6 children without gastrointestinal or malabsorption symptoms with hypertransaminasaemia of unknown cause. The liver biopsy of these patients showed different histopathological lesions ranging from reactive hepatitis to a moderately active chronic hepatitis.[9] GFD always led to normalisation of aminotransferase activity and to an amelioration of histological lesions in the two children who were re-biopsied. Gluten challenge after twelve months of GFD caused again an increase of serum aminotransferases in three other patients.

    Two retrospective studies in adults confirmed these findings, suggesting that up to 9% of patients with a persistent and cryptogenetic elevation of serum aminotransferases activity, may be affected by an asymptomatic CD.[10],[11]

    This reversible, gluten-related, liver damage today known as celiac hepatitis[12] is characterised by absence of any clinical sign or symptom suggesting a chronic liver disease and by mild, non-specific histological changes including Kupffer cell hyperplasia, mild lobular and portal tract inflammation or steatosis.

    Response to dietary treatment however, may be delayed up to 12 months; in such cases, an alternative diagnosis has to be considered.[2] In fact, less frequently, hypertransaminasemia may hide a severe chronic liver injury and even a cirrhosis.[5],[13] In these case, the histological features are consistent with an autoimmune liver damage including primary biliary cirrhosis (PBC) primary sclerosing cholangitis with overlap features and autoimmune hepatitis.[2] Actually, the prevalence of CD in adults with a chronic liver disease is at least 15-fold higher than in general population.[14] Moreover, the prevalence of CD in patients with autoimmune hepatitis was estimated to be 4% in a large population of adults[15](a prevalence eightfold higher than in general population) and similarly 3.4% among 96 children with autoimmune hepatitis at King's College, London, UK.[16] The converse, in a large multicentre study in children with CD, the prevalence of autoimmune hepatitis was found to be 1.1 %[17] and another study, recently performed in UK on 4732 adult patients with CD, demonstrated a threefold increase in risk for autoimmune cholestatic conditions, such as PBC and PSC, compared with controls.[18] In contrast to celiac hepatitis , autoimmune inflammatory liver injury do not seem to benefit from the institution of gluten-free diet by itself, but need a specific immunosuppressive therapy.[19]

    The pathogenetic mechanism of liver damage in celiac patients is poorly understood. The different types of liver injuries described may represent a spectrum of a same disorder where individual factors, such as genetic predisposition, precocity and duration of exposure to gluten may influence the reversibility of liver damage. Autoimmune liver disorders and CD share in fact common HLA class II haplotypes. In caucasian population, two haplotypes have been identified as susceptibility markers of autoimmune hepatitis: the complex HLA A1 B8 DR3 and the haplotype HLA DR4. Similarly, specific HLA class II antigens such as HLA-DR3, particularly the HLA-DQ2 molecule and HLA DR4, confer susceptibility to CD.[12], [20]

    Patients with celiac disease have an increased intestinal permeability which may facilitate the absorption of antigens from the gut. Increased permeability to intraluminal antigens could induce, in genetically predisposed individuals, an immune response both against antigens sharing common epitopes to self-liver-proteins and/or against cryptic antigens unmasked by the reaction with gliadin. It is known that mucosal damage in CD leads to exposure of tissue transgluta-minase enzyme, the target antigen recognised by anti-endomysial antibody. The hypothesis that this autoantibody may play a role in extraintestinal manifestations of CD and particularly in liver injury is supported by the recent finding of extracellular deposition of IgA class anti-tissue transglutaminase antibody in liver biopsy of two patients with active celiac disease.[21]

    Whether celiac disease is a potentially treatable cause of liver failure is currently debated.[22] A 4.3% prevalence of CD was recently found, in Finland, in a group of 185 adult patients who had undergone liver transplantation. The nature of the end-stage liver disease leading to liver transplantation in CD patients was in most cases, of autoimmune origin.[23] Furthermore, the authors report a dramatic improvement in liver function on a GFD in four untreated CD patients listed for liver transplantation, whom liver failure reversed on GFD, allowing 3 of them to escape to transplantation.[23] Similarly Ojetti et al . recently described an additional case of a 28 yr old woman with acute liver failure of unknown origin, found to be celiac during the enrolment into a transplant programme, in whom GFD by itself allowed her to restore liver function.[24] The occurrence in CD of a cryptogenic liver failure, requiring liver transplantation, has also been recently described during childhood.[25]

    These considerations recommend a rigorous cross-checking for a asymptomatic liver damage in CD individuals at diagnosis, and conversely, for CD by appropriate serology, in any cryptogenic liver disorder including end-stage liver failure and patients listed for liver transplantation.

    However in patients with chronic liver disease, attention should be paid, to the risk of false-positive results of serum anti-tissue transglutaminase, due to the different degree of specificity of the methods employed, to the high immunoglobulin concentration[26] and to the role of tissue transglutaminase in hepatic tissue repair.[27]

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