Gluten sensitivity is a systemic autoimmune disease with diverse manifestations. This disorder is characterised by abnormal immunological responsiveness to ingested gluten in genetically susceptible individuals. Coeliac disease, or gluten-sensitive enteropathy, is only one aspect of a range of possible manifestations of gluten sensitivity. Although neurological manifestations in patients with established coeliac disease have been reported since 1966, it was not until 30 years later that, in some individuals, gluten sensitivity was shown to manifest solely with neurological dysfunction. Furthermore, the concept of extraintestinal presentations without enteropathy has only recently become accepted. In this Personal View, we review the range of neurological manifestations of gluten sensitivity and discuss recent advances in the diagnosis and understanding of the pathophysiological mechanisms underlying neurological dysfunction related to gluten sensitivity.

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Gluten sensitivity: from gut to brain

Neurologic presentation of celiac disease.

From gut to brain

It has taken nearly 2000 years to appreciate that a common dietary protein introduced to the human diet relatively late in evolutionary terms (some 10 000 years ago), can produce human disease not only of the gut but also the skin and the nervous system. The protean neurological manifestations of gluten sensitivity can occur without gut involvement and neurologists must therefore become familiar with the common neurological presentations and means of diagnosis of this disease.

” . . .the stomach being the digestive organ, labours in digestion, when diarrhoea seizes the patient . . .and if in addition, the patient's general system be debilitated by atrophy of the body, the coeliac disease of a chronic nature is formed”.1 

This extract is from the book on chronic diseases by Aretaeus the Cappadocian, one of the most distinguished ancient Greek doctors of the first century AD. This chapter, entitled “on the coeliac diathesis”, was the first description of coeliac disease (from the greek word κ⊝ιλιακη meaning abdominal). Aretaeus' books were first published in Latin in 1500 and the new Latin word coeliac was used to translate κ⊝ιλιακη. Coeliac disease (CD) remained obscure until 1887 when Samuel Gee gave a lecture entitled On the coeliac affection 2 at the Hospital for Sick Children, Great Ormond Street, London. In it he acknowledged Areteaus' contribution and went on to give an accurate description of CD based on his own clinical observations.

With clinical manifestations primarily confined to the gastrointestinal tract or attributable to malabsorption, it was logical to assume that the target organ and hence the key to the pathogenesis of this disease was the gut. The first report of neurological manifestations associated with CD was by Carnegie Brown in 1908.3 In his book entitled Sprue and its treatment …

https://jnnp.bmj.com/content/jnnp/72/5/560.full.pdf

Gluten sensitivity as a neurological illness

Diagnosis of celiac sprue.

An association between celiac disease (CD) and other autoimmune diseases such as connective tissue diseases (CTD), inflammatory bowel diseases (IBD), and primary biliary cirrhosis (PBC) has been reported in several studies. However, a high rate of false positives in autoantibody testing was noted, especially when tissue transglutaminase (tTG) from guinea pig liver was used. Thus, the real prevalence of CD in CTD, IBD, and PBC is unclear. In a case-control study, 400 patients with CTD, 170 with IBD, 48 with PBC, and 120 healthy subjects were investigated for CD by the analysis of IgA and IgG tTG antibodies using the more specific human recombinant tTG immunoenzymatic assay. Patients and controls with positive findings were further tested for antiendomysial antibodies by indirect immunofluorescence and HLA typing, and those found positive by either of these tests underwent duodenal biopsy to confirm a possible diagnosis of CD. Twelve patients were positive for IgA or IgG tTG antibodies, showing an overall prevalence of 1.9%. Only 1 healthy subject (0.8%) had a low level positive reaction for IgA anti-tTG. Among the 12 patients and the healthy subject, only 2 (1 SLE and 1 ulcerative colitis patient) were subsequently confirmed to be affected with CD by positive EMA, HLA, and small bowel biopsy findings. The highest rate of false positives was found in PBC patients (10.4%). For these reasons, serological screening testing for CD is not recommended in CTD patients or in subjects affected with IBD or PBC, unless there is a relevant clinical suspicion of CD.

IgA and IgG tissue transglutaminase antibody prevalence and clinical significance in connective tissue diseases, inflammatory bowel disease, and primary biliary cirrhosis.

Gastrointestinal investigation of 14 adult patients with polymyositis disclosed coeliac disease in five. The inflammatory myopathy in our patients is not the same as the myopathy often seen in coeliac disease with osteomalacia. One patient has been free from both gastrointestinal and muscular symptoms for 5 years on a gluten-free diet alone. The findings strongly suggest an association between polymyositis and adult coeliac disease.

Polymyositis and adult coeliac disease

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Polymyositis and adult coeliac disease