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The safety of oats in the dietary treatment of coeliac disease

Published online by Cambridge University Press:  29 August 2012

Emile Richman*
Affiliation:
Department of Nutrition and Dietetics, Royal Liverpool University Hospital, Liverpool L7 8XP, UK
*
Corresponding author: fax+44 151 706 5980, email emile.richman@rlbuht.nhs.uk
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Abstract

Coeliac disease is a permanent inflammatory disorder of the small bowel affecting approximately 1% of the population. The only effective treatment that exists is exclusion of gluten from the diet. The present paper aims to review the literature as to whether oats are safe to eat for people with coeliac disease. Much data exist on the restrictive nature that adhering to a gluten-free diet imposes on an individual. If oats could be eaten, this would help reduce the restrictive nature of the diet. This in turn could lead to an increase in the quality of life. Oats are of high-nutritional value, providing a rich source of fibre, vitamins and minerals. The fibre source contains soluble fibre which is believed to help reduce LDL-cholesterol. A systematic review of the literature was conducted. Earlier studies conducted are difficult to compare as they used different methodologies and it is not known whether samples of oats in the studies were contaminated with gluten from other cereals. Many studies reviewed do not state the strain of oat used. Recent research has suggested that it may only be in certain strains of oats which could produce a toxic response to people with coeliac disease. In conclusion, research suggests that the risk from consuming oats may be less harmful than first thought; however, may vary according to the strain of oat. Handling that risk in clinical practice remains controversial.

Type
Conference on ‘Malnutrition matters’
Copyright
Copyright © The Author 2012

Introduction to coeliac disease

Coeliac disease is a chronic alteration of the proximal small intestines associated with a permanent intolerance of gluten in genetically susceptible people( Reference Corrazza 1 ). The disorder is highly diverse, ranging from asymptomatic to severely symptomatic. It is associated with numerous autoimmune disorders( Reference Haines, Anderson and Gibson 2 ). Whether consuming oats causes harm in coeliac disease is controversial for numerous reasons. There is a lack of consensus on the use of terms related to coeliac disease and gluten( Reference Fasano 3 ). This variability in the use of terminology has led to difficulty when comparing and evaluating clinical studies and research findings. In 2012, attempts were made to standardise terminology. This led us to a consensus statement from a working group in Oslo( Reference Ludvigsson, Leffler and Bai 4 ). This lack of definition has only added to the controversy of whether oats are harmful to people with coeliac disease.

Coeliac disease may well have a history dating back to the first and second centuries AD( Reference Losowsky 5 ). The first clear account of what might have been coeliac disease was by the physician Aretaeus of the first and second centuries AD, with his reference to undigested food, loose stools and ‘a coeliac disease of chronic nature’. The first clear description was given by Samuel Gee in 1888( Reference Gee 6 ). He suggested that dietary treatment might be of benefit. In the early twentieth century, various diets were tried, with some success, but without clear recognition of the toxic components. The doctoral thesis of Wim Dicke of 1950 established that exclusion of wheat, rye and oats from the diet led to dramatic improvement. The toxicity was shown to be a protein component, referred to as gluten( Reference Anderson and Marsh 7 ). Dicke's colleagues, Weijers and Van de Kamer, suggested that measurement of stool fat reflected the clinical condition.

Earlier studies were in children, but stool fat measurements documented that the condition could be recognised in adults. Histological abnormalities of the lining of the small intestine were demonstrated beyond doubt by Paulley in 1954( Reference Paulley 8 ). In 1956, techniques of biopsy of the jejunum were described by Shiner( Reference Shiner 9 ). Since 1954, serological and endoscopic techniques have improved the diagnosis of the condition.

Concurrence studies in monozygotic twins suggested a genetic component, confirmed by studies of human leucocyte antigens. The probability of developing coeliac disease if a first degree relative has coeliac disease is one in ten( 10 ). In addition, non-genetic factors (such as timing of gluten exposure) seem likely to contribute; however, the evidence is not conclusive( Reference Farrell and Kelly 11 ). Circulating antibodies suggest an immunological mechanism of damage and provide non-invasive screening tests. Osteoporosis is particularly associated with coeliac disease. Lymphoma, adenocarcinoma of the small intestine and a range of immunological disorders are also associated with coelaic disease. However, the risk of developing cancer from coelaic disease is low in absolute terms( Reference Holmes, Cassi and Fasano 12 ). A relationship with dermatitis herpetiformis was suggested by Samman in 1955 and established by Shuster and Marks in 1965 and 1968( Reference Reunala and Collins 13 ).

The only known effective treatment of coeliac disease is total exclusion of gluten from the diet. This can be extremely challenging to the patient( Reference Zarkadas 14 ) and cause a considerable burden. Non-adherence to a gluten-free diet has been shown to be as high as 58%( Reference Hall, Rubin and Charnock 15 ). Clearly, if oats were safe to eat, the diet would be less restrictive to many people and could well increase adherence. This has in turn been linked to a reduction in complications associated with coeliac disease( Reference Dickey 16 ). Research is being conducted using more convenient methods of treatment that are less restrictive than removing gluten from the diet. However, at present the only effective treatment that exists is adherence to a gluten-free diet.

It is clearly recognised in coeliac disease that the damage in the small bowel is induced in genetically susceptible people when proline- and glutamine-rich proteins found in wheat, barley and rye are eaten. However, knowledge on many aspects of the disorder is inadequate( Reference Mann and Leung 17 ). Present areas where information is lacking include definition of the tolerated levels of gluten among different individuals and the implication of non-adherence in people without classical symptoms. The exact prevalence of the condition is still not known. Another major area of controversy is whether oats are toxic for some or all people with coeliac disease. Debate has raged for decades as to whether proteins in oats cause similar damage to those of wheat, rye and barley.

Oats and coeliac disease

Oats, like all other grain varieties, belong to the Poaceae family. They are a staple in Germany, Ireland, Scotland and the Scandinavian countries. Avena sativa L (common oat) is the most important among the cultivated oats. Like wheat, it is an annual grass that is believed to be Asiatic in origin( Reference Masood, Butt and , Tahir-Nadeem 18 ). Modern oat, probably originated from the Asian wild red oat, which grew as a weed in other grain crops. Although the proteins in oats are similar to those in wheat, rye and barley, the oat prolamins (avenin) have significantly lower levels of proline( Reference Kilmartin, Lynch and Abuzakouk 19 ).

It is an annual crop used both for human and animal nutrition. Before being used as a food, it was used for medicinal purposes. Although oats are not suitable for bread making, they are found in a wide variety of foods and forms as well as being served as porridge. Thus, inclusion into a gluten-free diet would greatly expand the repertoire of foods that a person with coeliac disease could safely consume. There are a wide variety of cultivars which are characterised by their relative protein concentration. There are some traits that cause it to be less favoured than other grains. Many people find their taste bland and they have a shorter shelf life than many other cereal grains( Reference Olga, Gillespie and Zarkadas 20 ).

Despite these issues, oats contain numerous nutrients that have been shown to confer health benefits. Oat grains are a rich source of B-complex vitamins, proteins and minerals. Much attention has recently centred on their fibre content, in particular the soluble fibre content. This has been seen to be beneficial in the glycaemic control of people with diabetes. The β-glucan found in oats has also received much attention in particular, as it has been associated with improving lipid profiles, which have been linked with the prevention of heart disease.

Thus, the incorporation of oats into the diet is not only important from a quality of life standpoint for people with coeliac disease. They also have the potential to play a therapeutic role. As such, there is considerable relevance in knowing whether people with coeliac disease can eat oats safely.

Safety of oats

The first suggestion that oat consumption is deleterious in people with coelaic disease was made in 1953 when Van de Kamer measured fat absorption in a patient with coeliac diseases( Reference Van de Kamer, Weijers and Dickie 21 ). This sample size of one was clearly not statistically significant. It is unclear from early studies whether the samples of oats used were contaminated with gluten. At that time, technology did not exist to accurately assess traces of gluten.

Further studies were performed in other groups of children showing no harmful effects with oats( Reference Sheldon 22 ). However, these studies had less than six children and had numerous methodological flaws. There were no controls and indirect measurements were used for estimating damage to the gastrointestinal tract. No trial lasted more than 6 months from what is a life long condition. It is also difficult to compare accurately between these early studies as completely different methodologies were used( Reference Garsed and Scott 23 ).

With advances in histology more specific studies were performed. Haboubi et al.( Reference Haboubi, Taylor and Jones 24 ) in their systematic review report on six studies. Two of these six studies included in this review found changes in small bowel histology with increased intraepithelial levels in the group eating oats compared with the controlled group. However, in all six studies there was no significant difference in the serology between the control group and the oat group.

The largest study reported was by Janautuinen, who found no statistical difference in the grade of villous atrophy between the gluten-free diet with oats group and the standard gluten-free diet group in patients with coeliac disease in remission( Reference Janatuinen, Pikkarainen and Kemppainen 25 ). Janautuinen continued his earlier study( Reference Janatuinen, Kemppainen and Pikkarainen 26 ) for 5 years in an attempt to examine the long-term effects of a gluten-free diet containing oats in patients with coeliac disease. The authors contacted their original study population and discovered that after 5 years 65·7% of patients in the original oats group still consumed oats. Some patients who had reverted to a traditional gluten-free diet had done so because of concerns about the safety of oats at that time. The study showed an improvement in the villous architecture of both groups after 5 years. However, neither of the groups showed a return to normal. Thus, this proved inconclusive as to the safety efficacy of taking oats in coeliac disease.

These results differ slightly from the findings of the systematic review by Garsed and Scott in 2007( Reference Garsed and Scott 23 ). Using different inclusion and exclusion criteria they reviewed ten studies. From their review, they found only one out of 165 patients who showed mucosal damage from oat consumption. This one patient was added into a further uncontrolled study( Reference Arentz-Hansen, Fleckenstein and Molberg 27 ) which found two other patients who developed villous atrophy possibly caused by oats. As ever, it is difficult to be certain that gluten from wheat, rye and barley had not inadvertently entered into the diet of the subjects studied.

The methodology to assess potential pathology to oats is compounded by limited clinical tools of assessment. A reduction in symptoms does not guarantee absence of small bowel atrophy( Reference Kaukinen, Peraaho and Lindfors 28 ). The most widely used serological clinical test for coeliac disease is the presence of IgA tissue transglutaminase antibodies. If tissue transglutaminase levels are normal, it is still possible that the small bowel villi are still damaged( Reference Tursi, Brandimarte and Giorgetti 29 ). Subsequently, the testing of the reintroduction of oats using typical clinical assays becomes problematic.

However, a more recent study of the impact of oats using specific monoclonal antibodies showed more precise results( Reference Comino and Real 30 ). This research group demonstrated variation in response to different cultivars of oats. In this study, it was found that three groups of oat cultivars reacted differently against the monoclonal antibody moAb G12. The study distinguishes three groups of oat cultivars, which gave different reactions against the antibody: a group with considerable affinity, a group showing slight reactivity and another with no detectable reactivity. This suggests that the reactivity of this antibody with cereal storage proteins of different varieties of oats was correlated with its immunotoxicity. This gives an explanation for why only some oats trigger an immunological response. This is a rational hypothesis given that oats are a cereal crop that exists with a wide variety of form within the species. This would also explain different results from different studies performed. Many of the studies previously conducted do not mention the cultivar of oat used.

Current dietetic practice

There is clear discrepancy in the advice given regarding oats in clinical practice.

A recent survey of national societies for coeliac disease by Garsed in 2007( Reference Garsed and Scott 23 ) demonstrated clear variation in the advice given to their members. From the seven societies that replied to their survey, two recommended oats with caution (French speaking Switzerland and Slovenia). Five recommended against eating oats for people with coeliac disease (USA, Romania, South Africa, New Zealand and the society representing German and Italian speaking regions of Switzerland).

Further discrepancy also exists at a more local level. In three northwest England hospitals, three different policies on oat consumption exist. One hospital advises total avoidance of oats; one advises to try re-introduction after 6 months on a gluten-free diet. The third hospital advises re-introduction of oats after 12 months. The monitoring of patients after oat consumption also varied between the hospitals.

Conclusions

In reviewing the literature comparisons between different studies is extremely difficult not only due to the different study designs but also due to different conditions used in testing. There is also the issue of how the oat material used in the clinical trial has been tested for contamination of gluten. In view of recent studies particularly on oat cultivar( Reference Comino and Real 30 ), the whole area of accurate comparison has further been compounded as the vast majority of studies do not mention the variety of oat used.

This lack of clear evidence and controversy seen is highlighted by the different recommendations from different patient support groups. The controversy is exacerbated by the lack of clarity around terms relating to coelaic disease. The recent research on differing cultivars appears to shed more light on the extent of the risk of oat consumption. However, more research particularly in relation to cultivar variation is required to further clarify the risk of eating oats in coeliac disease. It is clear that if eating oats safely in coelaic disease is possible this would be of benefit to many patients. Given no 100% clear guidelines exist, it seems prudent as a minimum to clinically monitor patients who are eating uncontaminated oats.

Acknowledgements

The author thanks the staff at The Royal Liverpool University Hospital, in particular, Mr Peter Turner for his support and the librarians for their extremely swift response to requests for copies of journal articles. The author declares no conflicts of interest. No funding is declared.

References

1. Di Sabatino & Corrazza, GR (2009) Coeliac disease. Lancet 373, 14801493.Google Scholar
2. Haines, ML, Anderson, RP & Gibson, R (2008) Systematic review the evidence base for long-term management of coeliac disease. Aliment Phrmacol Ther 28, 10421066.Google Scholar
3. Fasano, A (2003) Celiac disease – how to handle a clinical chameleon. N Engl J Med 348, 25682570.Google Scholar
4. Ludvigsson, JF, Leffler, DA, Bai, JC et al. (2012) The Oslo definitions for coeliac disease and related terms. Gut Epublication ahead of print. doi: 10.1136/gutjnl-2011-301346.Google Scholar
5. Losowsky, MS (2008) A history of coeliac disease. Dig Dis 26, 112120.Google Scholar
6. Gee, SJ (1888) The coeliac affection. St Bartholomew's Hosp Rep 24, 1720.Google Scholar
7. Anderson, CM (1992) The evolution of a successful treatment of coeliac disease. In Coeliac Disease, pp. 8–10 [Marsh, editor MN]. London: Blackwell Scientific.Google Scholar
8. Paulley, JW (1954) Observations on the aetiology of idiopathic steatorrhoea. Br Med J 2, 13181321.Google Scholar
9. Shiner, M (1956) Duodenal biopsy. Lancet 1, 1719.Google Scholar
10. NICE (2009) Recognition and assessment of coeliac disease. CG86. London: National Institute for Health and Clinical Excellence.Google Scholar
11. Farrell, RJ & Kelly, PK (2002) Celiac sprue. N Engl J Med 346, 180188.Google Scholar
12. Holmes, G, Cassi, C & Fasano, A (2009) Fast Facts: Celiac Disease, 2nd ed., pp. 91–104. Oxford: Health Press.Google Scholar
13. Reunala, T & Collins, P (1997) Diseases associated with dermatitis herpetiformis. Br J Dermatol 159, 120124.Google Scholar
14. Zarkadas, M (2006) The impact of gluten free diet on adults with coeliac disease: results of a national survey. J Hum Nutr Diet 19, 4149.Google Scholar
15. Hall, NJ, Rubin, G & Charnock, A (2009) Systematic review: adherence to a gluten free diet in adults with coeliac disease. Aliment Pharmacol Ther 30, 315330.Google Scholar
16. Dickey, W (2008) Making oats safer for patients with coeliac disease. Eur J Gastroenterol Hepatol 20, 494495.Google Scholar
17. Mann, NS & Leung, JW (2006) Knowledge of some aspects of coeliac sprue among professors of gastroenterology. Intern Med J 13, 34.Google Scholar
18. Masood, S, Butt, M , Tahir-Nadeem, M et al. (2008) Oat: unique among the cereals. Eur J Nutr 47, 6879.Google Scholar
19. Kilmartin, C, Lynch, S, Abuzakouk, M et al. Avenin fails to induce a Th1 response in coeliac tissue following in vivo culture. Gut 52, 4752.Google Scholar
20. Olga, MP, Gillespie, G, Zarkadas, M et al. (2009) Introduction of oats in the diet of individuals with celiac disease: a systematic review. Adv Food Nutr Res 57, 235285.Google Scholar
21. Van de Kamer, JH, Weijers, HA & Dickie, WK (1953) Coeliac disease. An investigation into the injurious effects of the constituents of wheat in connection with their actions on patients with coeliac disease. Acta Paediatr 42, 223331.Google Scholar
22. Sheldon, W (1955) Coeliac disease. Lancet 269, 1097–1003.Google Scholar
23. Garsed, K & Scott, BB (2007) Can oats is taken in gluten free diet? A systematic review. Scand J Gastroenterol 42, 171178.Google Scholar
24. Haboubi, NY, Taylor, S, Jones, S (2006) Coeliac disease and oats: a systematic review. Postgrad Med J 82, 672678.Google Scholar
25. Janatuinen, EK, Pikkarainen, PH, Kemppainen, TA et al. (1995) A comparison of diets with and without oats in adults with celiac disease. N Engl J Med 333, 10331037.Google Scholar
26. Janatuinen, EK, Kemppainen, TA, Pikkarainen, PH et al. (2000) Lack of cellular and humoral immunological responses to oats in adults with coeliac disease. Gut 46, 327331.Google Scholar
27. Arentz-Hansen, H, Fleckenstein, B, Molberg, O et al. (2004) The molecular basis for oat intolerance in patients with celiac disease. PLoS Med 1, 8492.Google Scholar
28. Kaukinen, K, Peraaho, M, Lindfors, K et al. (2007) Persistent small bowel mucosal villous atrophy without symptoms of coeliac disease. Aliment Pharmacol Ther 25, 12371245.Google Scholar
29. Tursi, A, Brandimarte, G & Giorgetti, GM (2003) Lack of usefulness of antitransglutaminase antibodies in assessing histological recovery after gluten free diet in celiac disease. J Clin Gastroenterol 27, 387391.Google Scholar
30. Comino, I, Real, A, de Lorenzo et al. (2011) Diversity in oat potential immunogenicity: basis for the selection of oat varieties with no toxicity in coeliac disease. Gut 60, 915922.Google Scholar