Part 9 Of 12 Part Series: Psychological And Cognitive Symptoms With Undiagnosed Celiac Disease, Gluten Intolerance or Sensitivities

November 21, 2009 · Filed Under 12 Part Series: CD Symptoms 

This is the ninth in a series of posts discussing the variety of symptoms that can be caused by undiagnosed Celiac Disease (CD). In this post, psychological and cognitive symptoms will be discussed. There are studies, articles, and books identifying an association between CD/gluten sensitivities, psychological and cognitive symptoms  The pathogenesis is thought to be due to autoimmune reactions (to ingested gluten) causing inflammation and damage in the central nervous system (CNS) and the gastrointestinal tract in genetically predisposed individuals. With gastrointestinal involvement, nutrient deficiencies (common in CD), can add to the symptoms (1,5,6,10-12-14,15,19,20,23-29,32-34,37,38,41,42,55-57).

Many with psychological and cognitive symptoms associated with CD/gluten sensitivities do not have bowel symptoms. In others, the intestinal villi responsible for absorbing nutrients becomes damaged, creating a flattened mucosal surface (villous flattening). Autoimmune reactions to ingested gluten and related prolamines cross-react with intestinal villi and create this damage. Various nutrient deficiencies can occur and this can cause or add to the severity of the psychological and cognitive symptoms. Nutrient deficiencies contributing to psychological and cognitive symptoms can include vitamins A, B complex (esp. folic acid, B-6, and B12), D, E, K, essential amino and fatty acids (ex. tryptophan affects serotonin levels and low cholesterol associated with mental disorders), carbohydrates, low glucose (with associated diabetes), calcium, magnesium, phosphorus, copper, electrolytes, l-carnitine, and inositrol, and selenium (1,5,8,9,38,55,56).

Symptoms

The etiology and pathogenesis of psychological disorders and cognitive symptoms in CD/gluten sensitivities is unclear. It is reasonable to suspect that immunological reactions, inflammation, various neurological  abnormalities, and nutrient deficiencies may be responsible for the wide variety of psychological and cognitive symptoms. As well, enhanced production of cytokines in CD may stimulate the brain to produce neuroimmune, neuroendocrine, and neurochemical changes that may influence behavior. Pathological findings may include abnormal brain waves on electroencephalography (EEG), unusual cerebellar physiology, hypoperfused brain regions (also autoantibodies interferring with angiogenesis), brain atrophy, inflammation, patchy Purkinje cell (out-put neurons) loss in the cerebellum, and and progressive multifocal leukoencephalopathy (leading to destruction of myelin sheaths). As well, lymphocytic infiltration of the brain (along with associated vasculitis) could lead to glial, neuronal, or axonal damage. Other findings include widespread IgA deposition around vessels in the brain and brain white-matter lesions or calcifications, likely resulting from autoimmune reactions, calcium deposits, ischemia, vasculitis, or inflammatory demyelination (1,23,26,42,50-53,57-81). Collectively or individually, these factors may contribute to many psychological and cognitive symptoms. Many with undiagnosed CD (or gluten sensitivities) do not experience any psychological symptoms.

There are books, articles, and studies that identify an association between CD, gluten sensitivities, and depression ( 1,5,6,14,15,19,20,28,29,32,34,38,41,42-49,50-54,93). It is reasonable to suspect the central nervous system damage and inflammation combined with nutrient deficiencies (ex. low B vitamins, low serotonin and cholesterol) may be responsible. Other factors such as a sense of helplessness associated with being ill, misdiagnosed, or only having one’s symptoms diagnosed can certainly add to these feelings. Once diagnosed, depression might continue if underlying nutrient deficiencies are left untreated and unrecognized, if accidental ingestion of gluten occurs, if underlying food allergens are not identified, or if the individual has difficulty adjusting to a new lifestyle.  As well, personal coping strategies, adequate support and follow-up from healthcare professionals, family and friend supports, availability of gluten-free food and resources can all influence the outcome (1,38,22).

Learning disabilities are associated with undiagnosed CD (1,10-12,23,27,40,42). In books, articles, and studies, Attention Deficit Disorder (ADD) And Attention-Deficit/Hyperactivity Disorder (ADHD) is also associated with CD and gluten sensitivity (13,24,25,27,42). As well, subtle or obvious cognitive decline, dementia, can be linked to CD and gluten sensitivity (58,60,91,132). This could have long lasting effects on one’s life, affecting their confidence, self esteem, and can also decrease an individual’s ability to pursue the career of their choice since the cognitive effects may lead to poor academic performance.

In studies and articles, other psychological disorders have been associated with undiagnosed CD and gluten sensitivities, such as schizophrenia spectrum disorders (17,18,37,38,39,55,56,94-99), anxiety problems (1,32,33), mood disorders (14), apathy (33), sitophobia (abnormal aversion to food) (33), irritability (33,42), obsessional neurosis (38), anorexia/bulimia (33,42), and delinquent behavior (14,15,38). As well, there has been much controversy questioning a link between gluten and Autism and/or Asperger’s Syndrome. There are many reasons for this, I may compile a follow-up post at a later date on this topic. It certainly appears as if many have intestinal involvement, it seems reasonable to suspect that gluten, casein, and other possible food antigens may be involved. For now, I’ve provided links to more information at the end of the post.

I often felt like it was difficult to think, learn, and analyze. I managed to graduate from University with Honors. However, I was studying constantly to achieve that. I couldn’t seem to retain information very well. Now that I’m eating gluten-free, (along with corn, rice, and diary-free) my head finally feels clear and I can analyse and retain information with greater ease. I feel like it only takes about 1/3 of the time  to study now. It is difficult to learn when you are living with “Brain Fog”. My daughter, with CD, won an academic award last year. It may have been a very different outcome if she was still undiagnosed. She did have evidence of “brain fog” prior to diagnosis.

My middle child tested negative for CD. She had eczema of moderate severity, hyperactivity, lack of focus, occasional diarrhea, and abdominal discomfort. I was worried that she was experiencing some symptoms of ADHD. All medical tests ordered by the paediatric allergist were negative. An elimination diet revealed that she was sensitive to corn derivatives (which are in most grocery store products). All symptoms resolved when I removed corn from her diet. All symptoms return with accidental ingestion of corn derivatives. The hyperactivity and lack of focus is very pronounced with accidental ingestion of corn derivatives (ex. corn syrup, dextrose, glucose/fructose) which are in most processed foods.

Note: For more information, go to the links at the end of this post.

Influencing Factors

Other factors that may add to psychological and cognitive symptoms include hypothyroidism, adrenal disorders, diabetes, infections, low oxygen levels, hypotension, epilepsy, sleep disorders, genetics, a traumatic event, certain medications, poor diet, vitamin deficiency or toxicity, lack of resources, alcoholism, heavy metals, solvents, street drugs, and gastric surgery (leading to deficiencies) (1,2,3,8,9).

Diagnosis

There are a number of tests to consider when diagnosing gluten sensitivities. Anti-transglutaminase 6 IgA and IgG is prevalent in gluten ataxia and is useful to screen for gluten sensitivity in neurological disease (82). IgA endomysial antibodies and IgA anti-transglutaminase 2 tend to correspond with the severity of intestinal damage and is valuable along with an upper endoscopy with multiple biopsies to investigate intestinal involvement (1,5,6,82). A 2009 study recommends adding IgG Celiac G+ antibody test along with IgA anti-transglutaminase antibody for screening (83). If the patient has IgA deficiency then IgG tissue transglutaminase antibody test may be helpful. As well, IgG and IgA antigliadin antibodies may be helpful to identify if increased intestinal permeability has allowed gluten (gliadin) to leak in through the tight junctions between the intestinal epithelial cells. This leakage could potentially lead to a gluten sensitivity and with continued exposure potentially CD. Positive IgG and IgA antigliadin antibodies can indicate that a gluten sensitivity exists (1,5,6,64,84). In a 2008 study, Dr. Hadjivassiliou (neurologist) and colleagues recommend anti-transglutaminase 6 IgG and IgA, HLA genetic testing, IgG and IgA anti-gliadin antibodies, and anti-transglutaminase 2 antibodies to help identify gluten sensitivities in individuals with neurological disease (85).

Additional tests are available as well such as fecal tests, rectal mucosal patch technique (new in Sweden), and saliva tests. An MRI along with other neurological tests and biopsies may be ordered to investigate the pathological damage (1,5,6,78,86). It is important to explore the presence of nutrient deficiencies as well.

Do You Have Any Of The Above Symptoms?

CD can be present in children that are growing normally so normal growth rate should not be a factor that excludes the possibility of CD (87). Many individuals with undiagnosed CD/gluten sensitivities will have no bowel symptoms. Weight loss may or may not occur, and is dependent on the amount of the intestine that is damaged (1,2,3,9,88-90). Therefore, the symptoms in this post could occur in the absence of stunted growth, weight loss, or bowel symptoms.

The presence of psychological and cognitive symptoms as discussed in this post, indicates that you should talk to your MD about tests for gluten sensitivities/CD and tests to rule out other possible causes of your symptoms. Testing for CD/gluten sensitivities is important because undiagnosed CD increases the risk of developing other autoimmune diseases, lymphomas (skin, brain, lymph nodes, intestine), cancers (thyroid, esophageal, mouth, tongue, pharynx, tonsil, and small intestine), allergies, complications from malabsorption issues, possible decreased immune response to other illnesses (1,2,5,6,91), and many other health complications that will be discussed in the posts about CD/gluten sensitivity symptoms. It is my hope that if you have psychological or cognitive symptoms, you can print out this post complete with medical references to take with you to the MD when you request testing. Highlight or underline the sections that apply to your symptoms. I’ll be posting a simplified summary and checklist in the 12th post.

It is possible to have a gluten sensitivity even if you test negative for CD. It is also possible that some of your symptoms could be due to a food allergy/sensitivity or other disease process. For example, Dr. Stephen Wangen (http://tinyurl.com/yjsrqle) describes how a boy with TIC disorder benefited  a gluten-free, dairy-free diet (92). Allergy testing, and/or an elimination diet may help you to identify offending foods. Other tests can help rule out other diseases. I encourage everyone to have their symptoms thoroughly investigated by their MD and specialists before implementing a therapeutic diet. A consultation with a Registered Dietitian can provide guidance to ensure all nutritional needs are met. Keep your MD informed about any dietary changes you are making and also the results. Of course, I would love to hear your story as well.

I recommend waiting until CD/gluten sensitivity testing is complete before initiating a gluten-free diet because it may create a false negative. Discuss this with your MD or specialist. USE CAUTION WITH SUPPLEMENTS. Toxicities can occur with over supplementation and this can lead to permanent damage. Consult your MD, Registered Dietitian, or other medical specialists involved in your care to determine which nutrients should be supplemented and to identify appropriate dosages for you. Review your symptoms and everything in this post with a Medical Doctor and your specialists before you make any changes. Your MD knows your medical history and the treatments that are appropriate for you.

Diagnosed Celiacs and people with food allergies/sensitivities, please comment about your symptoms  and experiences at the end of each post. This will help other readers to see how the sometimes illusive symptoms of CD or food sensitivities can affect each of us.  We are all unique!

Links to more Information

1. Dr. Scot Lewey. Celiac Disease and gluten linked to brain disease by deposits in intestine and brain. http://tinyurl.com/yje7nv5

2. Dr. David Perlmutter, MD, FACN, ABIHM. Gluten sensitivity (Celiac Disease), ADHD, and other neurological problems in children. http://tinyurl.com/c2pzoo

3. Niederhofer H, Pittschieler K. A preliminary investigation of ADHD Symptoms In persons With celiac Disease.  http://jad.sagepub.com/cgi/content/abstract/10/2/200

4. Nathanel Zelnik MD, Avi Pacht MD, Raid Obeid MD, Aaron Lerner MD. Range of Neurological Disorders In Patients With Celiac Disease.  http://tinyurl.com/yjwaqrp

5. Elaine Gottschall. Recognizing Celiac behavior and catching it early by using SCD™ – would it prevent Autism? http://www.breakingtheviciouscycle.info/autism/dr_hass_exerpt.htm

6. Dr. Vikki Peterson. D.C., C.C.N. Gluten Sensitivity And Depression. http://tinyurl.com/bl7ox3

7. Ciacci C, Iovino P, Amoruso D, Siniscalchi M, Tortora R, Di Gilio A, Fusco M, Mazzacca G. Grown-up Coeliac Children: The Effects Of Only A Few Years On A Gluten-Free Diet In Childhood. http://www.ncbi.nlm.nih.gov/pubmed/15709993

8. The gluten connection: the association between schizophrenia and celiac disease.    http://www3.interscience.wiley.com/journal/118626206/abstract 

9. Findings in this study suggest that immune reactions in the intestine may affect individuals cognitively.  A J Wakefield FRCS et el. Enterocolitis in children with developmental disorders. http://www.nature.com/ajg/journal/v95/n9/abs/ajg2000579a.html

10. Ron Hoggan. Memory/Learning: Eating to Learn: How Grains Impact on Our Ability to Focus, Comprehend, Remember, Predict, and Survive. http://tinyurl.com/4nr67d

11. Prof. Rodney Ford M.B., B.S., M.D., F.R.A.C.P. Gluten Causes Brain Disease! http://tinyurl.com/naqvg9

12. Wendy Cohan, RN. Gluten, Celiac Disease and the Brain. http://tinyurl.com/d4z4c6

13. Ron Hoggan. ADD, Attention Deficit Hyperactivity Disorder – ADHD and Celiac Disease. http://tinyurl.com/ll9tpw

14. PA Pynnonen et el. Untreated Celiac Disease And Development Of Mental Disorders In Children And Adolescents.   http://psy.psychiatryonline.org/cgi/reprint/43/4/331.pdf 

15. Cholesterol is often low in undiagnosed Celiacs. Could the behaviour in this study be due to undiagnosed CD? Total serum cholesterol level, violent criminal offences, suicidal behaviour, mortality and the appearance of conduct disorder in Finnish male criminal offenders with antisocial personality disorder.  http://www.ncbi.nlm.nih.gov/pubmed/12056583

16. Cholesterol is often low in undiagnosed Celiacs. Could the behaviour in this study be due to undiagnosed CD?  Association of Serum Cholesterol and History of School Suspension among School-age Children and Adolescents in the United States. http://aje.oxfordjournals.org/cgi/content/abstract/161/7/691

17. Low Cholesterol and Mental Disorders in Children and Adolescents With Celiac Disease. http://psy.psychiatryonline.org/cgi/content/full/50/3/300

18. Part 1: Video (case study) about the neurological presentation of Celiac Disease in a baby. http://www.youtube.com/watch?v=Am6AUFVpKUk&NR=1

19. Part 2: Video (case study) about the neurological presentation of Celiac Disease in the same child as he became a toddler and preschooler. http://www.youtube.com/watch?v=TL_O-uInv3U&feature=related

Links for Autism

If you think your child may have CD/gluten sensitivities or other food sensitivities, consult your doctor for testing. A consultation with an Allergist for allergy testing may help to identify other allergies. A consultation with a Registered Dietician may help to ensure nutrient requirements are being met.

1. Substitutive and dietetic approaches in childhood autistic disorder: interests and limits”. http://www.ncbi.nlm.nih.gov/pubmed/19068339

2. Enterocolitis in children with developmental disorders.  http://www.nature.com/ajg/journal/v95/n9/abs/ajg2000579a.html

3. Wendy Cohan, RN. Gluten, Celiac Disease and the Brain. http://tinyurl.com/d4z4c6

4. Autistic disorder and gastrointestinal disease.  http://www.ncbi.nlm.nih.gov/pubmed/12352252?dopt=Abstract

5. Panenteric IBD-Like Disease in a Patient with Regressive Autism Shown for the First Time by the Wireless Capsule Enteroscopy: Another Piece in the Jigsaw of this Gut-Brain Syndrome? http://www3.interscience.wiley.com/journal/118681866/abstract

6. Focal-Enhanced Gastritis in Regressive Autism with Features Distinct from Crohn’s and Helicobacter Pylori Gastritis. http://www3.interscience.wiley.com/journal/118744704/abstract

7. The intestinal lesion of autistic spectrum disorder. http://www.ncbi.nlm.nih.gov/pubmed/16003130?dopt=Abstract

8. Differences between the gut microflora of children with autistic spectrum disorders and that of healthy children. http://www.ncbi.nlm.nih.gov/pubmed/16157555?dopt=Abstract

9. Oxidative stress in autism. http://tinyurl.com/yfwf6mh 

10. A Randomised, Controlled Study of Dietary Intervention in Autistic Syndromes. http://www.ncbi.nlm.nih.gov/pubmed/12168688 

11. Can the pathophysiology of autism be explained by the nature of the discovered urine peptides? http://www.ncbi.nlm.nih.gov/pubmed/12608733

12. Immune response to dietary proteins, gliadin and cerebellar peptides in children with autism. http://www.ncbi.nlm.nih.gov/pubmed/15526989

13. Jenny McCarthy http://www.generationrescue.org/autism/ and http://www.generationrescue.org/

References

1. Excellent Book: Green PHR, Jones, R. Celiac Disease A Hidden Epidemic. Collins, Harper Collins Publishers, 2006 http://tinyurl.com/ljeqjc

2. Pruessner Harold T, MD. Detecting Celiac Disease In Your Patients. American Family Physician. March 1st, 1998.

3. Feldman Mark, MD, Friedman Lawrence S, MD, Sleisenger, Marvin H, MD, Gastrointestinal and Liver Disease Pathophysiology/Diagnosis/Management 7th Edition, Volume11, 2002,Saunders

4. Barrett KE. Gastrointestinal Physiology. Lange Medical Books/McGraw-Hill 2006.

5. Excellent Book: Lieberman Shari PhD,CNC, FACN, with Linda Segall. The Gluten Connection. How Gluten Sensitivity May Be Sabotaging Your Health. Rodale Inc., 2007. http://tinyurl.com/nwsc79

6. Excellent Book: James Braly, MD., Ron Hoggan, MA. Dangerous Grains. Penguin Group, Inc., 2002. http://tinyurl.com/knswhn 

7. Medicinenet.com. How Are Malabsorption And Malnutrition Evaluated In Celiac Disease. http://www.medicinenet.com/celiac_disease/page7.htm#tocp

8. Gibney MJ, Marinos E, Olle L, Dowsett J. Clinical Nutrition. Blackwell Publishing 2005.

9. Gibney MJ, Vorster HH, Kok FJ. Introduction to Human Nutrition. Blackwell Publishing 2002.

10. Ron Hoggan. Memory/Learning: Eating to Learn: How Grains Impact on Our Ability to Focus, Comprehend, Remember, Predict, and Survive. http://www.celiac.com/articles/711/1/MemoryLearning-Eating-to-Learn-How-Grains-Impact-on-Our-Ability-to-Focus-Comprehend-Remember-Predict-and-Survive-by-Ron-Hoggan/Page1.html

11. Prof. Rodney Ford M.B., B.S., M.D., F.R.A.C.P. Gluten Causes Brain Disease! http://www.celiac.com/articles/1085/1/Gluten-Causes-Brain-Disease-By-Prof-Rodney-Ford-MB-BS-MD-FRACP/Page1.html

12. Wendy Cohan, RN. Gluten, Celiac Disease and the Brain. http://www.celiac.com/articles/21635/1/Gluten-Celiac-Disease-and-the-Brain/Page1.html

13. Ron Hoggan. ADD, Attention Deficit Hyperactivity Disorder – ADHD and Celiac Disease. http://www.celiac.com/articles/110/1/ADD-Attention-Deficit-Hyperactivity-Disorder—ADHD-and-Celiac-Disease/Page1.html

14. Ludvigsson JF, Reutfors J, Osby U, Ekbom A, Montgomery SM. Coeliac disease and risk of mood disorders–a general population-based cohort study. J Affect Disord. 2007 Apr;99(1-3):117-26. Epub 2006 Oct 6.

15. Pynnönen PA, Isometsä ET, Aronen ET, Verkasalo MA, Savilahti E, Aalberg VA. Mental disorders in adolescents with celiac disease. Psychosomatics. 2004 Jul-Aug;45(4):325-35.

16. Päivi A Pynnönen,corresponding author1 Erkki T Isometsä,2 Matti A Verkasalo,1 Seppo A Kähkönen,3 Ilkka Sipilä,1 Erkki Savilahti,1 and Veikko A Aalberg1 Gluten-free diet may alleviate depressive and behavioural symptoms in adolescents with coeliac disease: a prospective follow-up case-series study. BMC Psychiatry. 2005; 5: 14.

17. William Eaton, professor,1 Preben Bo Mortensen, professor,2 Esben Agerbo, assistant professor,2 Majella Byrne, assistant professor,2 Ole Mors, associate professor,3 and Henrik Ewald, professor3 Coeliac disease and schizophrenia: population based case control study with linkage of Danish national registers. BMJ. 2004 February 21; 328(7437): 438–439.

18. Bryan D Kraft1 and Eric C Westmancorresponding author2 Schizophrenia, gluten, and low-carbohydrate, ketogenic diets: a case report and review of the literature. Nutr Metab (Lond). 2009; 6: 10.

19. O. Dhodanand Kowlessar,† Lorraine J. Haeffner,‡ and Gordon D. Benson§ Abnormal Tryptophan Metabolism in Patients with Adult Celiac Disease, with Evidence for Deficiency of Vitamin B6*. J Clin Invest. 1964 May; 43(5): 894–903.

20. M I Torres,* M A López-Casado,† P Lorite,* and A Ríos‡ Tryptophan metabolism and indoleamine 2,3-dioxygenase expression in coeliac disease. Clin Exp Immunol. 2007 June; 148(3): 419–424.

21. Ciacci C, Iovino P, Amoruso D, Siniscalchi M, Tortora R, Di Gilio A, Fusco M, Mazzacca G. Grown-up coeliac children: the effects of only a few years on a gluten-free diet in childhood. Aliment Pharmacol Ther. 2005 Feb 15;21(4):421-9.

22. Signs and symptoms of Depression http://www.nimh.nih.gov/health/publications/depression/complete-index.shtml#pub3

23. Dr. Scot Lewey. Celiac Disease and gluten linked to brain disease by deposits in intestine and brain. Ezine Articles. http://tinyurl.com/yje7nv5

24. Dr. David Perlmutter, MD, FACN, ABIHM. Gluten sensitivity (Celiac Disease), ADHD, and other neurological problems in children. http://tinyurl.com/c2pzoo

25. Niederhofer H, Pittschieler K. A preliminary investigation of ADHD Symptoms In persons With celiac Disease. Journal of Attention disorders, 2006 Nov;10(2):200-4. http://jad.sagepub.com/cgi/content/abstract/10/2/200

26. G Addolorato, DD Giuda, GD Rossi, V Valenza, et el. Regional cerebral hypoperfusion in patients with celiac disease. The American Journal of Medicine, Volume 116, Issue 5, Pages 312-317

27. Nathanel Zelnik MD, Avi Pacht MD, Raid Obeid MD, Aaron Lerner MD. Range of Neurological Disorders In Patients With Celiac Disease. Pediatrics Vol. 113 No. 6 June 2004, pp.1672-1676. http://tinyurl.com/yjwaqrp

28. Ciacci C, Iavarone A, Mazzacca G, De Rosa A: Depressive symptoms in adult coeliac disease. Scand J Gastroenterology 1998; 33:247–250

29. Hallert C, Martensson J, Allgen LG: Brain availability of monoamine precursors in adult coeliac disease. Scand J Gastroenterol 1982; 17:87–89

30. Hallert C, Derefeldt T: Psychic disturbances in adult coeliac disease, I: clinical observations. Scand J Gastroenterol 1982; 17:17–19

31. Hallert C, Åström J, Walan A: Reversal of psychopatology in adult coeliac disease with the aid of pyroxidine (vitamin B6). Scand J Gastroenterol 1983; 18:229–304

32. Addolorato G, Stefanini GF, Capristo E, Caputo F, Gasbarrini A, Gasbarrini G: Anxiety and depression in adult untreated celiac subjects and in patients affected by inflammatory bowel disease: a personality "trait" or a reactive illness? Hepatogastroenterology 1996; 43:1513–1517.

33. Elaine Gottschall. Recognizing Celiac behavior and catching it early by using SCD™ – would it prevent Autism? http://www.breakingtheviciouscycle.info/autism/dr_hass_exerpt.htm

34. Dr. Vikki Peterson. D.C., C.C.N. Gluten Sensitivity And Depression. http://tinyurl.com/bl7ox3   www.celiac.com

35. Hjiej H, Doyen C, Couprie C, Kaye K, Contejean Y. Substitutive and dietetic approaches in childhood autistic disorder: interests and limits. Encephale. 2008 Oct;34(5):496-503. Epub 2008 Mar 4.

36. Päivi A. Pynnönen, M.D., Erkki T. Isometsä, M.D., Ph.D., Matti A. Verkasalo, M.D., Erkki Savilahti, M.D., Ph.D., and Veikko A. Aalberg, M.D., Ph.D. Untreated Celiac Disease and Development of Mental Disorders in Children and Adolescents. Psychosomatics 43:331-334, August 2002.

37. A J Wakefield FRCS1,2, A Anthony PhD, MBBS, MSc2, S H Murch PhD, FRCP, FRCPCH3, M Thomson MBChB, MRCP, FRCPCH3, S M Montgomery PhD2, S Davies MRCPath2, J J O’Leary MD, DPhil, MRCPath4, M Berelowitz FRCPsych5 and J A Walker-Smith MD, FRCP, FRACP, FRCPCH3  Enterocolitis in children with developmental disorders. The American Journal of Gastroenterology (2000) 95, 2285|[ndash]|2295; doi:10.1111/j.1572-0241.2000.03248.x http://www.nature.com/ajg/journal/v95/n9/abs/ajg2000579a.html

38. Luca Mascitelli, M.D., Medical Service Comando Brigata Alpina "Julia" Udine, Italy, Francesca Pezzetta, M.D., Cardiology Service Ospedale di Tolmezzo Tolmezzo, Italy, and Mark R. Goldstein, M.D., Fountain Medical Court Bonita Springs, FL United States. Low Cholesterol and Mental Disorders in Children and Adolescents With Celiac Disease. Psychosomatics 50:300-301, May-June 2009

39. William W. Eaton, Ph.D., Majella Byrne, Ph.D., Henrik Ewald, Dr.Med.Sc., Ole Mors, Ph.D., Chuan-Yu Chen, Ph.D., Esben Agerbo, M.S., and Preben Bo Mortensen, M.D., Dr.Med.Sc. Association of Schizophrenia and Autoimmune Diseases: Linkage of Danish National Registers. Am J Psychiatry 163:521-528, March 2006. http://ajp.psychiatryonline.org/cgi/content/abstract/163/3/521

40. Ron Hoggan. Memory/Learning: Eating to Learn: How Grains Impact on Our Ability to Focus, Comprehend, Remember, Predict, and Survive. http://www.celiac.com/articles/711/1/MemoryLearning-Eating-to-Learn-How-Grains-Impact-on-Our-Ability-to-Focus-Comprehend-Remember-Predict-and-Survive-by-Ron-Hoggan/Page1.html www.celiac.com 

41. O. Dhodanand Kowlessar,† Lorraine J. Haeffner,‡ and Gordon D. Benson§  Abnormal Tryptophan Metabolism in Patients with Adult Celiac Disease, with Evidence for Deficiency of Vitamin B6*  J Clin Invest. 1964 May; 43(5): 894–903.

42. PA Pynnonen, ET Isometsa, MA Verkasalo, E Savilahti, VA Aalberg. Untreated Celiac Disease And Development Of Mental Disorders In Children And Adolescents.  Psychosomatics 43:331-334, August 2002. http://psy.psychiatryonline.org/cgi/reprint/43/4/331.pdf

43. Hallert C, Derefeldt T. Psychic disturbances in adult coeliac disease. I. Clinical observations. Scand J Gastroenterol. 1982 Jan;17(1):17-9. http://www.ncbi.nlm.nih.gov/pubmed/7134833

44. Hallert C, Aström J. Psychic disturbances in adult coeliac disease. II. Psychological findings. Scand J Gastroenterol. 1982 Jan;17(1):21-4. http://www.ncbi.nlm.nih.gov/pubmed/7134834

45. Hallert C, Aström J, Sedvall G. Psychic disturbances in adult coeliac disease. III. Reduced central monoamine metabolism and signs of depression. Scand J Gastroenterol. 1982 Jan;17(1):25-8.

46. C. CIACCI, A. IAVARONE, G. MAZZACCA, A. DE ROSA. Depressive Symptoms in Adult Coeliac Disease. Scandinavian Journal of Gastroenterology 1998, Vol. 33, No. 3, Pages 247-250

47. Hallert C, Sedvall G. Improvement in central monoamine metabolism in adult coeliac patients starting a gluten-free diet. Psychol Med. 1983 May;13(2):267-71.

48. A Hernanz and I Polanco. Plasma precursor amino acids of central nervous system monoamines in children with coeliac disease. Gut. 1991 December; 32(12): 1478–1481. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1379246/

49. Smith KA, Fairburn CG, Cowen PJ. Relapse of depression after rapid depletion of tryptophan. Lancet. 1997 Mar 29;349(9056):915-9.

50. LAHAT, SHAPIRO, KARBAN, GERSTEIN, KINARTY & LERNER. Cytokine Profile in Coeliac Disease. Scandinavian Journal Of Immunology, Volume49 Issue 4, Pages 441-447.

51. Olga J.G. Schiepers, Marieke C. WichersCorresponding Author Contact Information, E-mail The Corresponding Author and Michael Maes. Cytokines and major depression. Progress in Neuro-Psychopharmacology and Biological Psychiatry. Volume 29, Issue 2, February 2005, Pages 201-217.

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