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    Dr. Ron Hoggan, Ed.D.
    Dr. Ron Hoggan, Ed.D.

    An Experts Group Meeting About Non-celiac Gluten Sensitivity

    Reviewed and edited by a celiac disease expert.

    Journal of Gluten Sensitivity Winter 2014 Issue

    An Experts Group Meeting About Non-celiac Gluten Sensitivity - CC--ITU/I.Wood
    Caption: CC--ITU/I.Wood

    This article originally appeared in the Winter 2014 issue of Journal of Gluten Sensitivity.

    Celiac.com 04/30/2014 - Dr. Catassi and colleagues reported, in the September of 2013 issue of Nutrients, that during the previous 21 months for every ten reports about celiac disease, there was one report of non-celiac gluten sensitivity (1).  They plotted the publication ratio over the last 60+ years, showing that there has been a steady increase of reports on non-celiac gluten sensitivity in the medical literature that has grown proportionally faster than the number of reports about celiac disease, and most of us are aware of the rapid growth made by the celiac literature during that same period. By implication, we may reasonably assume that this reflects a growing interest among physicians and other health care workers.  Catassi and colleagues mention the first meeting of an expert panel in London during 2011, and report on discussions from the December, 2012 meeting of experts in Munich, addressing a wide range of illnesses thought to have some connection with gluten ingestion (1, 2).  An approximately concurrent report by Mooney et al ( including Sanders, one of the above-mentioned experts) (3)  attempts to clarify and extend some of the information from the Catassi et al report, as well as contradicting it on the issue of IgG anti-gliadin antibodies as a potential biomarker for non-celiac gluten sensitivity (1).   This growing trend of interest in non-celiac gluten sensitivity, along with the publications specifically cited here, offer enormous affirmation of the Journal of Gluten Sensitivity and its editorial staff, and we are loathe to criticize it in any way.

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    However,  in the same report, Catassi and colleagues repeatedly decry the “lack of biomarkers” for non-celiac gluten sensitivity (1). In essence, they  are saying that there is no known laboratory test that will reliably identify this form of gluten sensitivity. Further, while they admit that they have “poor knowledge of the pathophysiology” of non-celiac gluten sensitivity, they seem to assume that oats may be safely eaten by individuals afflicted by this sensitivity. They appear to reflexively exclude oats from any further investigation, as a possible factor in non-celiac gluten sensitivity. Such assumptions appear to be bleeding over into their perceptions of non-celiac gluten sensitivity from their work with celiac disease.    

    The IBS Connection
    Catassi et al also cite one study that reports a rate of 28% of non-celiac gluten sensitivity among IBS patients, and a larger study that reports a rate of 30% of IBS patients who have wheat sensitivity, either with or without other food sensitivities.  This same group reports a prevalence of IBS in northern Europe of between 16%  and 25% of the population (1).  If we take their most conservative numbers,  estimating that IBS afflicts only 16% of the population, and that 28% of that group has  non-celiac gluten sensitivity, then about 4.48% of northern Europeans should have non-celiac gluten sensitivity. Catassi et al  say that the rate could well be above 1% (1). Some might suggest that this is a gross understatement that distorts the data rather than clarifying it. This, too, may reflect a preoccupation with lessons learned from celiac disease, rather than a de novo view of gluten sensitivity.  

    They cite yet another study of a subset of IBS patients in which diarrhea was the predominant symptom, particularly among patients with genetic HLA DQ2 and DQ8 markers, which are associated with celiac disease.  These IBS patients showed compromised bowel barrier function when consuming gluten, presumably as a function of barrier permeability.  They go on to assert that the gluten free diet offers some measure of symptom relief even to those patients whose IBS may be partly or wholly driven by low-fermentable, poorly-absorbed, short-chain carbohydrates, as  gluten proteins may be included in this list of potentially problematic foods.  

    Psychiatric Connections
    Catassi and colleagues also explore schizophrenia and autism  where sub-groups of non-celiac gluten sensitivity have been identified. They report the findings of two studies of schizophrenic patients wherein no benefits were seen after gluten avoidance over the study periods of either 10 days (4) or 5 weeks of treating 8 chronic schizophrenic patients (5).  Catassi et al also mention the mildly positive results from a study of 14 weeks’ duration (6). However, beyond citing one paper authored by Dr. Curtis Dohan, identified as the earliest suggestion of a connection between gluten and schizophrenia, they do not mention the recommendations of Dohan and his colleagues, who called for a minimum study duration of at least six months and as much as a year on a gluten free, dairy free diet before the potential benefits of this diet can be observed in schizophrenic patients.  They also recommended treating newly diagnosed and newly relapsed schizophrenic patients with this diet as they had observed little positive response among the chronic schizophrenic subjects they studied (8, 9, 10, 11). Further,  Catassi et al completely fail to acknowledge the work by Zioudrou and colleagues (12) that identifies a possible source of urinary peptides seen both in many schizophrenics (13, 14) and many patients with autism (15). These peptides have, since their discovery, been recognized as psychoactive (12).  These insights are particularly important in these realms of mental illness and abnormal development, as they offer insights that may someday offer vastly more effective treatments than are currently available.  Again, celiac disease may be coloring the lens through which these experts are looking at non-celiac gluten sensitivity.   

    Catassi and his colleagues go on to acknowledge that IgG class antibodies against gliadin, a sub-group of gluten proteins, as markers for increased intestinal permeability (1) but they fail to acknowledge this protein group as the missing “biomarker” of gluten sensitivity. They say:  “Non-celiac gluten sensitivity is currently a diagnosis of exclusion with the only positive diagnostic criterion being the clinical response to gluten withdrawal. Patients should have negative celiac serology, normal duodenal histology, and negative IgE-based tests” (1).  

    IgG against gliadin offers a biomarker for 19.8% tp 23.5% of the population.  Yet serology is the most common approach to measuring IgG anti-gliadin, and others have made this connection, identifying IgG class anti-gliadin antibodies as “ a measure of the immune response to gliadin” (7). (Gliadin is a sub-group of gluten proteins.)  If  someone is mounting an immune response against gliadin, it is reasonable to say that they are gluten sensitive. So why would Catassi and colleagues back away from the data suggesting that non-celiac gluten sensitivity may afflict from 4.48% to as many as 7.5% of the northern European population, based only on those with diagnosed IBS?  Further, 12%  of healthy blood donors in the United Kingdom  have also been reported to show elevated levels of anti-gliadin antibodies (16).  Taken together, these suggest a rate of non-celiac gluten sensitivity, as identified by IgG class antibodies against gliadin among northern Europeans, of between 16.8% and 19.5%  of the general population.  

    Dr. Sapone and her group have identified and reported on a group of non-celiac gluten sensitive patients (21) who present with what Dr. Sapone and her group have  elsewhere characterized as a function of the innate immune system and comprise between 6% and 7%  of the general population (22).  Only about half of these subjects show anti-gliadin antibodies but since they are not healthy blood donors or IBS patients, we may reasonably predict that between 22.8% and 26.5% of the population has non-celiac gluten sensitivity.  

    And there are likely a lot more cases than are suggested by those numbers.   For instance, about 7% of patients with multiple sclerosis showed IgG class antibodies against gliadin (17),  while more than 20% of patients with Crohn’s disease, and 6.5% of patients with rheumatoid arthritis also showed elevated IgG antibodies against gliadin (18), and Samaroo et al found the same antibodies elevated in the sera of 5.6% of the schizophrenic  patients they studied (19).   And Hadjivassiliou’s group states “IgG antigliadin antibodies have a high sensitivity not only for patients with coeliac disease but also for those with minimal or no bowel damage where the principal target organ is the cerebellum or peripheral nervous system” (20).  

    Cancer
    Perhaps the most distressing part of the Catassi report is where it says “No major complication of NCGS has so far been described; especially autoimmune comorbidity , as observed in celiac disease, has not been reported so far.” In 2007, Anderson et al published a report in which people with non-celiac gluten sensitivity experienced: “ ..... the incidence of malignant neoplasms in patients with celiac disease (positive EMA test) was similar to that of the Northern Ireland population. However,  mortality from malignant neoplasms, NHL [non-Hodgkin’s lymphoma], and digestive system disorders was significantly increased in patients who were gluten sensitive with a negative EMA test” (7).  This same report states that it may be the first investigation of malignancy and mortality among non-celiac gluten sensitive patients (7) and they have found that cancer and increased mortality is higher among those who are gluten sensitive than among those with celiac disease.  

    Why Not IgG Anti-gliadin as Biomarkers?
    You may, like me, be wondering why the Catassi-led group retreated from the use of IgG antibodies against gliadin as a bio-marker for gluten sensitivity, when the consequences of ignoring it are made obvious by the Anderson et al study  mentioned in the previous paragraph, showing increased mortality rates in this group. This result may be due to physicians’ failure to recommend a gluten free diet, reflecting their skepticism regarding this marker.  The Catassi et al skepticism is especially puzzling when at least one of their own members (Sanders) had submitted a report for publication at about the same time, in which he and his colleagues assert a prevalence of non-celiac gluten sensitivity of 12%, among healthy blood donors, based on IgG anti-gliadin antibodies  (3).   We are also left wondering why these experts would ignore the recommendations and insights embodied in the large and earliest body of research connecting schizophrenia and gluten, authored by Curtis Dohan and his colleagues (8-14) while Catassi et al seem to give credence to the negative results reported by investigations lasting only ten days or five weeks?

    I think that Catassi et al have answered this question, but before we discuss that, I’d like to point out that elite athletes have reported improved performance on a gluten free diet (23, 24). They were already performing at the very pinnacle of their sports, yet their experimenting with the gluten-free (and in one case, also a paleo-diet) led to enhanced performance.  That really is quite amazing.  And what about those with IgG AGA who have neurological or other autoimmune diseases?  Also, the girl that Kim and I wrote about in the last issue of this Journal is a perfect example of a patient with autoimmune diabetes, where celiac disease was ruled out, so she was told that she would have to inject insulin for the rest of her life. Yet all she needed was a gluten free diet and very insightful parents who were willing to press physicians to expand their thinking a little.

    I must say that I am very pleased with Catassi et al’s stated recognition of extra-intestinal manifestations of non-celiac gluten sensitivity.  However, their approach is to call for further characterizing  the various groups that respond differently to gluten, based on grouping by specific illnesses. This may miss the larger picture.  Catassi et al acknowledge that “The vast majority of celiac experts initially reacted with a great deal of skepticism to the concept of NCGS existence and the fact that it was a separate entity from celiac disease” (1).  They go on to suggest that we are about at the same place that we were forty years ago with celiac disease.  Perhaps.  

    As it stands, we have celiac disease and we have non-specific anti-gliadin antibodies that signal the lion’s share of cases of non-celiac gluten sensitivity, an increased risk for autoimmunity, a majority of a wide range of neurological diseases that are also more frequent among those with celiac disease, we also have many children with ADHD who recover on a gluten-free diet alone, we have a very large majority of children with learning disabilities who recover on a strict gluten-free diet, we have people who lose weight on a gluten-free diet, we have people who just think that they feel better on a gluten-free diet, and we have elite athletes who perform better on a gluten free diet.  We also have cases of non-celiac gluten sensitivity as characterized by Dr. Sapone et al, where the innate immune system is involved, and we only have anti-gliadin antibodies associated with about half of those individuals.   

    When we see all these fractured pieces scattered about the landscape of gluten induced illness, it is highly likely that we are missing the larger vista that incorporates all of them. But we would have to let go of some sacred cows to see that larger picture. The first sacred cow we should abandon is the idea of celiac disease as a distinct and most important disease entity, and begin to think of gluten induced disease, or to use Rodney Ford’s term, “gluten syndrome”.   I think it is great that non-celiac gluten sensitivity is getting more recognition, but the current lens through which medical researchers view celiac disease and non-celiac gluten sensitivity may be clouded by their reductionist  paradigm.

    The problem, as I see it, is that celiac disease has long been mischaracterized. When Dr. Dicke showed that the gluten free diet reversed celiac disease, few believed him.  He was laughed out of a world conference in New York City and vowed never to return to the USA.  When he and his colleagues searched for a ‘scientific’ way to validate the diet as an effective treatment for celiac disease, they  found intestinal villous atrophy, so the medical understanding of gluten induced illness has evolved, primarily, as an intestinal ailment characterized by villous atrophy.  

    I think that Dr. Rodney Ford’s conception of celiac disease as a sub-group of intestinal and extra-intestinal ailments that first derive from gluten’s assault on neurological tissues (25) is better rooted in the facts, and much more likely to prove true.  Ford’s perspective may well provide a better tool for understanding gluten’s impact on human health - although it impugns major parts of more than seventy years of medical and scientific research into celiac disease. It may even suggest that we were looking in the wrong direction for much of the time. Ford postulates that gluten’s first insult is to neurological tissues. Those who are susceptible to celiac disease may go on to develop intestinal damage as a sequel to the neurological injury. Those who are not susceptible to celiac disease may go on to develop any of a number of gluten-related ailments, depending on their unique genetic makeup, experiences, and exposures (25).  Understandably, Rodney’s conception may be unpopular among some medical practitioners and researchers - but it sure fits the facts better than anything else I’ve seen.   

    Sources:  

    1. Catassi C, Bai JC, Bonaz B, Bouma G, Calabrò A, Carroccio A, Castillejo G, Ciacci C, Cristofori F, Dolinsek J, Francavilla R, Elli L, Green P, Holtmeier W, Koehler P, Koletzko S, Meinhold C, Sanders D, Schumann M, Schuppan D, Ullrich R, Vécsei A, Volta U, Zevallos V, Sapone A, Fasano  A. Non-Celiac Gluten Sensitivity: The New Frontier of Gluten Related Disorders. Nutrients 2013, 5, 3839-3853.
    2. Open Original Shared Link
    3. Mooney PD, Aziz I, Sanders DS. Non-celiac gluten sensitivity: clinical relevance and recommendations for future research. Neurogastroenterol Motil. 2013 Nov;25(11):864-71. doi: 10.1111/nmo.12216. Epub 2013 Aug 12.
    4. Storms LH, Clopton JM, Wright C. Effects of gluten on schizophrenics. Arch Gen Psychiatry. 1982 Mar;39(3):323-7.
    5. Potkin SG, Weinberger D, Kleinman J, Nasrallah H, Luchins D, Bigelow L, Linnoila M, Fischer SH, Bjornsson TD, Carman J, Gillin JC, Wyatt RJ. Wheat gluten  challenge in schizophrenic patients. Am J Psychiatry. 1981 Sep;138(9):1208-11.
    6. Vlissides DN, Venulet A, Jenner FA.A double-blind gluten-free/gluten-load controlled trial in a secure ward population.Br J Psychiatry. 1986 Apr;148:447-52.
    7. Anderson LA, McMillan SA, Watson RG, Monaghan P, Gavin AT, Fox C, Murray LJ. Malignancy and mortality in a population-based cohort of patients with coeliac disease or “gluten sensitivity”. World J Gastroenterol. 2007 Jan 7;13(1):146-51.
    8. Dohan “Cereals and schizophrenia: data and hypothesis” Acta Psychiat Scand 1966; 42: 125-152
    9. Dohan et. al. “Relapsed Schizophrenics: More Rapid Improvement on a Milk-and Cereal-free Diet” Brit J Psychiat 1969; 115: 595-596
    10. Dohan et. al. “Is Schizophrenia Rare if Grain is Rare?” Biol Psychiat 1984; 19(3): 385-399
    11. Dohan “Is celiac disease a clue to pathogenesis of schizophrenia?” Mental Hyg 1969; 53: 525-529
    12. Zioudrou et. al. “Opioid peptides derived from food proteins. The exorphins” J Biol Chem 1979; 254:2446-2449
    13. Dohan FC. Genetic hypothesis of idiopathic schizophrenia: its exorphin connection. Schizophr Bull. 1988;14(4):489-94.
    14. Severance EG, Alaedini A, Yang S, Halling M, Gressitt KL, Stallings CR, Origoni AE, Vaughan C, Khushalani S, Leweke FM, Dickerson FB, Yolken RH. Gastrointestinal inflammation and associated immune activation in schizophrenia. Schizophr Res. 2012 Jun;138(1):48-53.
    15. Reichelt KL, Tveiten D, Knivsberg AM, Brønstad G.Peptides’ role in autism with emphasis on exorphins.Microb Ecol Health Dis. 2012 Aug 24;23.
    16. Hadjivassiliou M, Gibson A, Davies-Jones GA, Lobo AJ, Stephenson TJ, Milford-Ward A.Does cryptic gluten sensitivity play a part in neurological illness? Lancet. 1996 Feb 10;347(8998):369-71.
    17. Shor DB, Barzilai O, Ram M, Izhaky D, Porat-Katz BS, Chapman J, Blank M, Anaya JM, Shoenfeld Y. Gluten sensitivity in multiple sclerosis: experimental myth or clinical truth? Ann N Y Acad Sci. 2009 Sep;1173:343-9. doi: 10.1111/j.1749-6632.2009.04620.x.
    18. Shor DB, Orbach H, Boaz M, Altman A, Anaya JM, Bizzaro N, Tincani A, Cervera R, Espinosa G, Stojanovich L, Rozman B, Bombardieri S, Vita SD, Damoiseaux J, Villalta D, Tonutti E, Tozzoli R, Barzilai O, Ram M, Blank M, Agmon-Levin N, Shoenfeld Y. Gastrointestinal-associated autoantibodies in different autoimmune diseases. Am J Clin Exp Immunol. 2012 May 25;1(1):49-55. Print 2012.
    19. Samaroo D, Dickerson F, Kasarda DD, Green PH, Briani C, Yolken RH, Alaedini A. Novel immune response to gluten in individuals with schizophrenia. Schizophr Res. 2010 May;118(1-3):248-55. doi: 10.1016/j.schres.2009.08.009. Epub 2009 Sep 11.
    20. Hadjivassiliou M, Grünewald RA, Davies-Jones G A B. Gluten sensitivity: a many headed hydra. Heightened responsiveness to gluten is not confined to the gut. BMJ. 1999 June 26; 318(7200): 1710–1711.
    21. Sapone A, Lammers KM, Casolaro V, Cammarota M, Giuliano MT, De Rosa M, Stefanile R, Mazzarella G, Tolone C, Russo MI, Esposito P, Ferraraccio F, Cartenì M, Riegler G, de Magistris L, Fasano A. Divergence of gut permeability and mucosal immune gene expression in two gluten-associated conditions: celiac disease and gluten sensitivity. BMC Med. 2011 Mar 9;9:23.
    22. Sapone A, Lammers K M, Mazzarella G, Mikhailenko I, Cartenì M,  Casolaro V, Fasano A. Differential Mucosal IL-17 Expression in Two Gliadin-Induced Disorders: Gluten Sensitivity and the Autoimmune Enteropathy Celiac Disease. Int Arch Allergy Immunol. 2010 April; 152(1): 75–80. Published online 2009 November 24.
    23. https://www.celiac.com/articles/23375/1/New-Djokovic-Book-Promotes-Gluten-free-Diet/Page1.html 
    24. Open Original Shared Link
    25. Ford RPK. The gluten syndrome: a neurological disease. Medical Hypotheses. 2009:73, 438-440


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    Guest Dr Rodney Ford

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    What an excellent commentary on this very important topic. Yes, the authors needs to be congratulated for putting this paper together. I totally agree with Dr Ron Hoggan that the authors have gone out of their way to be as conservative as possible about the value of the AGA and the proportion of the population who have gluten sensitivity. Remember that a decade ago, these gastroenterologists scoffed at the concept of gluten sensitivity - and now at last they have recognised that it is a real and common entity. In another few years they will be more confident to embrace gluten sensitivity in all of its guises.

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  • About Me

    Dr. Ron Hoggan, Ed.D.

    As co-author of "Dangerous Grains" and "Cereal Killers", the study of the impact of gluten continues to be a driving passion in my life. I am fascinated by the way that gluten induces illness and impedes learning while it alters mood, behavior, and a host of other facets of our existence. Sure, the impact of gluten on health is an important issue, but that is only the most obvious area of impact. Mood disturbances, learning disabilities, and the loss of quality of life due to psychiatric and neurological illness are even more tragic than the plethora of physical ailments that are caused or worsened by gluten. The further I go down this rabbit hole, the more I realize that grains are a good food for ruminants - not people. I am a retired school teacher. Over the last decade, I have done some college and university level teaching, but the bulk of my teaching career was spent working with high school students.


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