June 2009 Issue

Understanding Celiac Disease
By John Libonati and Cleo Libonati, RN, BSN
Today’s Dietitian
Vol. 11 No. 6 P. 50

Suggested CDR Learning Codes: 5110, 5120, 5210, 5220, 5290; Level 2

Celiac disease is a debilitating autoimmune disorder that affects an estimated 1% of the world’s population, including more than 3 million Americans. Only a small percentage of these people are currently diagnosed, but recent improvements in testing methods and greater public and professional awareness are expected to increase diagnoses by tenfold during the next few years.1 Because treatment is dietary, dietitians can expect to see a substantial increase in clients with celiac disease. This article will help dietitians identify the symptoms of nutrient deficiencies associated with celiac disease and provide guidance to meet their clients’ nutritional needs.

Celiac disease is an inherited, immune-mediated intolerance to dietary gluten. “Gluten” is the collective term for the amino acid sequences found in wheat, barley, rye, and, to a lesser extent, oats (see sidebar), which trigger an immune reaction.2 When gluten is ingested, susceptible individuals mount a specific, intense inflammatory response within the small intestinal mucosa that damages the lining and interferes with digestion and absorption.

The condition has the potential to produce a broad range of symptoms, associated disorders, and complications that may affect any organ or body system. It can be activated at any time after a susceptible person begins to eat gluten-containing foods. Gluten sensitivity is lifelong and cannot be outgrown. While gluten itself is the environmental cause for development of antibodies, certain stressors can trigger active disease, including gluten overload, pregnancy, viral or bacterial infection, surgery, overexercise, and severe stress, according to the National Institutes of Health.

Pathophysiology
Gluten resists digestion, yielding protein fragments that can disrupt the mucosal barrier system that normally prevents large molecules from slipping through the intestinal lining. Gluten fragments penetrating the intestinal lining are deamidated, or modified, by the intestinal enzyme tissue transglutaminase to form a complex that stimulates the immune system to produce antibodies, which then attack the complex within the submucosa. The ensuing inflammation swells the mucosa and damages its delicate structures, causing varying degrees of villous atrophy and crypt hyperplasia, thus preventing the proper digestion and absorption of multiple nutrients, leading to malnutrition. Malnutrition brings about malfunction in those body systems requiring the deficient nutrient(s), and hundreds of health problems may result.

Celiac disease potentially encompasses many disorders in systems outside the digestive tract that compound the adverse effects of malnutrition. For example, brain atrophy and diminished brain perfusion stem from the effect of gluten itself. Anxiety and depression result from nutrient deficiencies. The compounding effect of the loss of brain tissue and diminished perfusion with anxiety and depression would have a major impact on cognitive function and emotional stability.

Malabsorption occurs and can persist for some time before there is biopsy evidence of mucosal damage—histology can appear normal, but the person’s health can be at risk. Postdiagnostic testing to evaluate the response to treatment may show a return to normal histology, yet malabsorption could persist.

The clinical outcome depends on the duration of exposure. The longer gluten is consumed, the more the body is damaged and the greater the likelihood of health disorders and complications.3 There is no cure at present. The treatment is the elimination of gluten from the diet, known as the gluten-free diet.

Symptoms
There are no “typical” symptoms of celiac disease. It was traditionally thought that people with celiac disease were underweight, but the body of evidence shows that the average patient presents with a normal body mass index, and overweight patients are more prevalent than underweight patients. Manifestations vary with the individual, may appear at any time in life after the introduction of gluten, and may be intestinal or extraintestinal (see Table 1).

Intestinal enzyme deficiencies, sugar intolerances, and associated dysbiosis appear commonly in patients with celiac disease.4 Research indicates that the metabolic activity of intestinal microbial flora in those with celiac disease is different from the general population and that it is a genuine phenomenon of celiac disease not affected by either the diet, the inflammation, or the autoimmune status of the patient.5 The severity of disturbances in intestinal balance of flora is found to depend on the gravity of the patient’s state.6

Nutrient deficits are responsible for most symptoms in celiac disease; many are seemingly unrelated conditions. A partial list includes depression, an inability to concentrate, anxiety, insomnia, hypertension, obesity, anorexia, nonalcoholic fatty liver disease, secondary hyperparathyroidism, idiopathic hypoparathyroidism, alopecia, defective fingernails, edema, eczema, seborrhea, muscle abnormalities, ataxia, tremors, brain atrophy, dementia, headache, chronic fatigue, peripheral neuropathy, cataracts, blurred vision, bone pain, infertility, dysmenorrhea, male impotence, miscarriage, obstetrical complications, chromosomal aberrations, spina bifida, angina pectoris, cardiomegaly, atherosclerosis, osteoporosis, osteomalacia, and prolonged or repeat infections.3

Childhood presentations include chronic diarrhea, hypotonia, failure to thrive, growth retardation, short stature, convulsions, poor bone and tooth development, thymic atrophy, delayed puberty, hematological abnormalities, refractory iron deficiency anemia, attention-deficit/hyperactivity disorder, developmental delay, behavioral disorders, cognitive disorders, social disorders, stroke, juvenile idiopathic arthritis, juvenile autoimmune thyroid disease, juvenile diabetes, osteopenia, rickets, and cancer predisposition.3

Gastrointestinal Problems
Celiac disease causes many gastrointestinal health problems. It disrupts the action of muscles, nerves, reflexes, enzymes, and hormones and interferes with digestive function, causing the malabsorption of nutrients. Effects are noted throughout the GI tract:

• Hunger: Loss of appetite, or anorexia, can result from just one nutrient deficiency or a combination of deficiencies. These nutrients include zinc, iron, magnesium, phosphorus, potassium, thiamin, vitamin B12, and protein. Increased thirst results from omega-3 fatty acid or potassium deficiencies.3

• Mouth: Lowered saliva pH (more acidic saliva) associated with celiac disease predisposes a person to dental caries and poor starch digestion. Dental caries may develop from a deficiency of calcium in saliva composition. Dental enamel defects include demarcated opacities and hypoplasia, yellowing, and horizontal grooves or pits on permanent teeth. The pathogenesis is not clearly understood, but the damage occurs before the crowns of permanent teeth have developed.

Painful aphthous and nonaphthous mouth ulcers are frequently associated with celiac disease. These can be due to folic acid, iron, and vitamin B12 deficiencies or direct contact with gluten. Gingival inflammation, bleeding, and eventual tooth loss from infection result from vitamin C deficiency.

Cracking at the mouth corners, burning lips and mouth, and magenta tongue (with hypertrophy or atrophy of papillae) result from riboflavin deficiency. A pale, sore, and swollen tongue results from iron deficiency, while niacin deficiency causes a scarlet, swollen tongue with burning of the mouth. A beefy red, smooth tongue with burning results from vitamin B12 deficiency.

Oral inflammation results from folic acid and vitamin B6 deficiency. Increased susceptibility to infection results from iron and vitamin A deficiencies, while impaired taste results from zinc, vitamin B12, and niacin deficiencies.

• Pharynx: Niacin deficiency can cause burning of the throat. Dysphagia can be caused by iron deficiency, and laryngospasm can be caused by calcium, magnesium, and vitamin D3 deficiencies.

• Esophagus: Dysphagia, gastroesophageal reflux disease, and esophageal motor abnormalities are common. Burning of the esophagus and heartburn can be caused by niacin deficiency. Plummer-Vinson Syndrome, a type of dysphagia, is caused by iron deficiency.

• Stomach: Delayed gastric emptying, poor protein digestion due to low hydrochloric acid levels causing low pepsin output, gastric ulcerations, and lymphocytic and collagenous gastritis are observed.

Nausea and vomiting result from magnesium, potassium, and niacin deficiencies. Indigestion results from thiamin deficiency. Increased permeability of gastric mucosa, resulting in increased susceptibility to ulcer-causing Helicobacter pylori bacterial infection, is exacerbated by iron and niacin deficiencies.

• Small intestine: The malabsorption of nutrients such as fat, protein, carbohydrate, minerals, and vitamins can occur and is made worse by folic acid deficiency. Loss of membrane integrity of the gastrointestinal lining, thickening of epithelial cells, and increased susceptibility to microbe invasion result from vitamin A deficiency. Sugar intolerances include lactose, sucrose, and maltose.

Abdominal distention results from gas, intestinal edema, and niacin deficiency. Abdominal pain results from inflammation, spasm, gas, and thiamin and vitamin B12 deficiencies. Steatorrhea is a consequence of fat malabsorption. Acute onset diarrhea can be due to zinc deficiency. Chronic diarrhea results from poorly absorbed nutrients and deficiencies of niacin and folic acid and is made worse by zinc deficiency and potassium depletion. Intermittent diarrhea and constipation result from vitamin B12 deficiency.

Intestinal edema results from inflammation. Increased intestinal permeability of small intestinal mucosa causing increased susceptibility to Candida albicans mucosal infection is enhanced by iron, omega-3 fatty acid, vitamin A, and vitamin C deficiencies.

Bovine beta casein enteropathy, development of food allergies, lymphocytosis, adenocarcinoma of small intestine, cryptic intestinal T-cell lymphoma (refractory sprue), and enteropathy-associated T-cell lymphoma are observed.

• Duodenum: The malabsorption of minerals includes calcium, chloride, fluoride, sulfur, iron, copper, magnesium, and zinc. The diminished active transport of calcium, magnesium, zinc, and other minerals across the gut and the reduced absorption result in part from vitamin D deficiency. Fat malabsorption binds minerals, causing loss in the feces and loose bowels or diarrhea. Pancreatic insufficiency results in fat malabsorption. Scalloping of the duodenal folds, duodenal erosions and ulceration, postbulbar duodenal ulceration, and stenosis are observed.

• Jejunum: Inflammation causes maldigestion and malabsorption of protein, carbohydrate, fat, vitamins C and B6, thiamin, riboflavin, and folic acid. Jejunal ulceration and chronic ulcerative jejunitis are observed.

• Ileum: Inflammation causes malabsorption of amino acids, monosaccharides, and vitamins A, D, E, K, and B12.

• Colon: Common symptoms include constipation alternating with diarrhea, constipation resulting from deficiencies in thiamin and vitamin B12, gas from niacin deficiency, and irritable bowel syndrome. Crohn’s disease may be exacerbated by omega-3 fatty acid and zinc deficiencies. Collagenous, lymphocytic, and ulcerative colitis may be exacerbated by omega-3 fatty acid and vitamin A deficiencies; occult gastrointestinal bleeding can result from vitamin C and K deficiencies. 

Treatment
Treatment is a strict gluten-free diet—wheat, barley, rye, and oats are excluded—for life. Dietary treatment should result in the rapid improvement or prevention of most manifestations, provided nutritional deficiencies are attended.

Once gluten is eliminated, surface cells of the mucosal lining are replaced within five days. Swelling of the lining subsides in about two weeks, and intestinal permeability improves within two months. Villi structures regenerate within six months but can take five years or more in some cases. Lactose, sucrose, and maltose intolerances improve as villi regain enzyme function.7

The gluten-free diet must be strict to be effective. How much gluten is too much? People vary in their tolerance. Studies show that 25 mg gliadin protein in wheat per day produces symptoms and intestinal changes, but as little as 1 mg/day has been reported to prevent healing; 20 mg gliadin equals 1/8 tsp of flour.

Because of the effects on digestion and absorption, deficiencies of vitamins, minerals, proteins, carbohydrates, and essential fatty acids should be addressed. At diagnosis, baseline serology of vitamins A, D, E, K, B12, and folic acid and the minerals iron, calcium, and phosphorus should be obtained. Mild cases may not require supplementation; severe cases may require comprehensive nutritional replacement.1

Specific health issues require lab testing or procedures for proper treatment. For example, osteoporosis calls for vitamin D and calcium levels, bone enzymes, and yearly bone density scans.

Despite a good clinical response, abnormal endoscopic and histologic appearances persist in the majority of patients.8 Research shows that baseline education of patients significantly predicts dietary compliance and intestinal damage at follow-up.9 Intervention that uncovers hidden celiac disease, provides nutritional education, and promotes regular follow-up will considerably improve prognosis.

The gluten-free diet is challenging due to the ubiquitous presence of gluten-containing food in the standard American diet. Education is critically important to help clients meet lifestyle needs. Patients need detailed diet instruction, including how to read food labels and identify hidden sources of gluten (eg, medications and supplements). Each client must understand and participate in his or her diet design and treatment planning. The steps include the following:

• Avoid gluten. Educate the client as necessary to ensure that he or she understands what gluten is, where it is found, and how to avoid it. Education should include safe food preparation techniques, reading ingredient labels, and recognizing overt and hidden sources of gluten.

• Identify nutrient deficiency symptoms. People grow accustomed to being unwell and may not report problems—they may never have experienced wellness. Interviews and questionnaires are the best methods for eliciting client symptoms. Direct observation and review of medical history will reveal manifestations.

• Incorporate deficient nutrients into the diet. Determine which symptoms are due to nutrient deficiencies and incorporate the missing nutrients into the diet plan.

• Meet lifestyle needs. The healthy client understands the gluten-free diet, consumes the foods that his or her body needs, and is comfortable with maintaining the diet in all areas of life: eating out, travel, social activities, food shopping, dating, school, etc. Participation in a celiac disease support group is an effective means of promoting adherence to a gluten-free diet and may provide emotional and social support.

Dietary Sources of Nutrients
It is preferable to obtain the needed nutrients from food sources rather than from supplements. Because of the ubiquitous presence of gluten, this can be difficult, and deficiencies can result that must be corrected. The following food sources should aid professionals with designing a healthy gluten-free diet that fits the individual’s nutritional needs:

• Glucose: Carbohydrate sources include honey, syrups, all edible disaccharides, fruits, vegetables, and starches.

• Protein: Rich animal sources include meat, poultry, seafood, fish, eggs, and dairy. Rich plant sources include tree nuts, soybeans, peanuts, legumes, and seeds.

• Omega-3 fatty acids:
Alpha-linolenic acid: A rich source is flaxseed meal or oil. Good sources are soybean oil, canola oil, walnuts, butternuts, red and black currant seeds, chia seeds, soybeans, and dark green vegetable leaves.

DHA: Highest sources are salmon oil, cod liver oil, menhaden oil, and herring oil. Good sources are Atlantic mackerel, Muroaji scad, bluefin tuna, king mackerel, lake trout, albacore tuna, lake whitefish, Atlantic salmon, sprat, anchovy, Atlantic herring, and bluefish. Human milk contains DHA, but cow’s milk does not.

EPA: The highest sources are menhaden fish oil, cod liver oil, salmon oil, and herring oil. Rich sources are fatty marine fish: sardines in oil, Pacific herring, mackerel, Chinook salmon, sablefish, Atlantic herring, Atlantic sturgeon, halibut, sockeye salmon, anchovy, and mullet. Lesser amounts are in high–omega-3 eggs, common periwinkle, conch, and Pacific oyster.

• Omega-6 fatty acids:
Arachidonic acid (AA): The body can produce AA, while dietary sources include meat and dairy products. AA is also a component of breast milk.

Linoleic acid: Rich sources include vegetable oils: safflower, corn, sunflower, and ground nut. Plant sources include nuts, seeds, soy products, fortified orange juice, broccoli, bok choy, and green leafy vegetables such as turnip greens, beet greens, collards, kale, and dandelion.

• Minerals:
Calcium: Rich plant sources include fortified orange juice, bok choy, rice, English walnuts, and green leafy vegetables such as collards, turnip greens, beet greens, and dandelion. Animal sources include milk and dairy products, canned salmon, sardines, and crab.

Copper: Rich animal sources include meat, organs, and shellfish. Plant sources include chocolate, nuts, brown rice, legumes, and dried fruits.3

Iron: Rich animal sources include liver, oysters, seafood, organ meats, meat, fish, poultry, and egg yolks. Iron from plant sources is not well absorbed, but good sources include brown rice, legumes, gluten-free fortified cereal, and wines.

Magnesium: Rich plant sources include soybeans, buckwheat, black-eyed peas, almonds, cashews, kidney beans, lima beans, Brazil nuts, pecans, gluten-free whole grains, peanuts, walnuts, and bananas. Rich animal sources are halibut and haddock, with lesser amounts in other fish, shellfish, and chicken.

Phosphorus: Good animal sources include dairy products and liver, with lesser amounts in crabmeat, beef, chicken, clams, and fish. Very rich plant sources include peanuts, almonds, cashews, walnuts, filbert nuts, macadamia nuts, and pecans. Good amounts are in chickpeas, lentils, lima beans, cocoa, and chocolate.

Potassium: Good animal sources are dairy, beef, poultry, and fish. Plant sources are much higher, the richest sources being dried figs, dates, parsley, soybeans, bamboo shoots, mushrooms, beet greens, raisins, tree nuts, plantains, potatoes, and winter squash. Good sources are bananas, beans, pumpkin, chickpeas, and endive.

Selenium: The richest source is the Brazil nut. Richest animal sources are kidney, tuna, oysters, liver, clams, dark turkey meat, fish, and shrimp. A rich plant source is sunflower seeds.

Zinc: The highest animal source is the oyster. Rich meat sources include canned salmon, beef, liver, turkey neck, shellfish, poultry, and fish. Good plant choices include soybeans, pumpkin seeds, dry peas, dry beans, brown rice, and sunflower seeds.

• Vitamins (fat soluble):
Vitamin A: Rich sources are found in preformed animal foods. Liver is the highest source, followed by oysters, cod, and halibut. Good sources are milk, cheese, butter, eggs, and fish. Plants are sources of carotenoids, and exceptionally rich sources include pumpkin, carrots, and sweet potatoes. Excellent vegetables are dark green leafy plants such as beet greens, spinach, and broccoli, as well as yellow-orange fruits such as cantaloupe, oranges, peaches, and apricots.

Vitamin D: Rich animal sources include fish liver oil and egg yolks. Very good sources include herring, salmon, mackerel, sardines, tuna, fortified milk, and butter.

Vitamin E: Animal sources are low, with the most amounts in salmon, butter, and chicken. Rich plant sources include sunflower oil, almonds, corn oil, avocados, olive oil, beans, apricots, plant leaves, and brown rice.

Vitamin K: Animal sources are low; beef and pork are best. Rich plant sources include green leafy vegetables such as broccoli, cabbage, turnip greens, spinach, seaweed, and dark lettuce.

Vitamin B1 (Thiamin): Rich animal sources include pork, milk (whole or 2%), salmon, halibut, chicken, beef, and eggs. Plant sources include pecans, sunflower seeds, filberts, walnuts, watermelon, chestnuts, beans, peanuts, avocados, peas, and whole grain rice.

• Vitamins (water soluble):
Vitamin B2 (Riboflavin): Sources include liver, milk, yogurt, clams, eggs, pork, cheese, beef, chicken, trout, brewer’s yeast, spinach, brown rice, oranges, and apples.

Vitamin B3 (Niacin): The richest animal source is liver. Good sources include oysters, milk, yogurt, clams, pork, cheese, beef, chicken, eggs, human milk, and trout. The richest plant source is almonds. Good sources include brewer’s yeast, black-eyed peas, spinach, peanuts, chestnuts, avocados, asparagus, broccoli, soybeans, beans, brown rice, and orange juice.3

Vitamin B6 (Pyridoxine): Animal sources are more available for absorption than plant sources and include beef liver, chicken, halibut, pork, beef, milk (whole or 2%), and eggs. Good plant sources include bananas, potatoes, avocados, sunflower seeds, brown rice, prunes, white rice, peanut butter, Brussels sprouts, oranges, cauliflower, tomatoes, and apples.3

Vitamin B9 (Folic acid): The richest animal source is liver, followed by lamb and veal. Good sources are beef, egg yolk, shrimp, oysters, clams, and cheese. Plant sources are rich in folates, especially lentils, beans, chickpeas, spinach, turnip greens, black-eyed peas, active dry yeast, broccoli, asparagus, collard greens, avocados, oranges, and green leafy vegetables.

Vitamin B12: Rich animal sources include clams, beef liver, oysters, crab, tuna, beef, halibut, 2% milk, pork, eggs, cheese, chicken, and yogurt. Plant sources include some sea vegetables.

Vitamin C: Rich sources include orange juice, fresh broccoli, citrus fruits, papaya, strawberries, yellow peppers, kiwi, cantaloupe, honeydew, and cranberry juice.

Continuing Problems
Unintentional gluten ingestion is the most common reason for continuing problems. A food diary is useful to identify sources of contamination. Lack of adherence to the gluten-free diet is another problem, especially in those who do not exhibit obvious symptoms after consuming gluten. Reasons for nonadherence must be uncovered, and methods must be provided that enable the client to properly adhere to the diet.

After eliminating gluten from the diet, persisting deficiencies in celiac disease may be due to slow or incomplete healing of the small intestine, failure to eat foods rich in needed nutrients, eating too much fiber with meals, thus binding nutrients, or H. pylori infection, small bowel bacterial overgrowth, giardia, or other infections or parasites.

Celiac disease presents a unique opportunity for dietitians because diet is the only effective treatment. Education, assistance in planning, and properly identifying and correcting nutrient deficiencies will deliver the best health outcome for clients with celiac disease.

— John Libonati and Cleo Libonati, RN, BSN, are cofounders of Gluten Free Works, Inc and publishers of the celiac disease reference Recognizing Celiac Disease, www.glutenfreeworks.com, and www.recognizingceliacdisease.com. John Libonati is also president-elect of the Celiac Sprue Association.

References
1. National Digestive Diseases Information Clearinghouse. Celiac Disease. September 2008. NIH Publication No. 08-4269.

2. Celiac Sprue Association. Celiac Disease: The Basics. 2005 version 2.2008.

3. Libonati CJ. Recognizing Celiac Disease: Signs, Symptoms, Associated Disorders & Complications. Fort Washington, Pa.: Gluten Free Works, Inc; 2007.

4. Tjellström B, Stenhammar L, Högberg L, et al. Gut microflora associated characteristics in children with celiac disease. Am J Gastroenterol. 2005;100(12):2784-2788.

5. Murray IA, Smith JA, Coupland K, Ansell ID, Long RG. Intestinal disaccharidase deficiency without villous atrophy may represent early celiac disease. Scand J Gastroenterol. 2001;36(2):163-168.

6. Kamilova AT, Akhmedov NN, Pulatova DB, Nurmatov BA. [Intestinal microbiocenosis in children with intestinal enzymopathy.] Zh Mikrobiol Epidemiol Immunobiol. 2001;(3):97-99.

7. Cummins AG, Thompson FM, Butler RN, et al. Improvement in intestinal permeability precedes morphometric recovery of the small intestine in coeliac disease. Clin Sci (Lond). 2001;100(4):379-386.

8. Lee SK, Lo W, Memeo L, Rotterdam H, Green PH. Duodenal histology in patients with celiac disease after treatment with a gluten-free diet. Gastrointest Endosc. 2003;57(2):187-191.

9. Ciacci C, Cirillo M, Cavallaro R, Mazzacca G. Long term follow-up of celiac adults on gluten-free diet: Prevalence and correlates of intestinal damage. Digestion. 2002;66(3):178-185.

Learning Objectives
After completing this exercise, the student will be able to:

1. Explain why celiac disease has been underdiagnosed.

2. Explain the etiology of celiac disease.

3. Explain why there are no “typical” symptoms of celiac disease.

4. Understand and discuss common problems associated with gluten intolerance.

5. Explain why nutritional deficiencies cause most problems associated with celiac disease.

6. Discuss the effects of celiac disease on the gastrointestinal tract and relate them to nutritional deficiencies.

7. List four steps of celiac disease treatment.

Examination
1. Celiac disease is:
a. genetic.
b. autoimmune.
c. multisystem.
d. All of the above

2. The average client with celiac disease:
a. is underweight.
b. is overweight.
c. has a normal body mass index.
d. There is no average body weight.

3. ___________ can trigger active celiac disease.
a. Pregnancy
b. Gluten overload
c. Stress
d. All of the above

4. Celiac disease symptoms first present in:
a. infancy.
b. childhood.
c. adulthood.
d. anytime following dietary introduction of gluten.

5. Symptoms are an accurate indicator of whether someone with celiac disease has consumed gluten.
a. True
b. False

6. Symptoms of celiac disease:
a. can change over time.
b. are always gastrointestinal.
c. are the same for all people.
d. All of the above

7. Typical symptoms of celiac disease include:
a. diarrhea.
b. migraines.
c. constipation.
d. There are no typical symptoms.

8. At diagnosis, baseline serology of the following vitamins and minerals should be obtained:
a. A, D, E, K, B12, folic acid, iron, calcium, and phosphorus
b. C, E, zinc, and magnesium
c. A, D, E, B6, and folic acid
d. Iron, calcium, phosphorus, and thiamin

9. Surface cells of the intestine regenerate in:
a. five days.
b. two weeks.
c. six months.
d. five years.

10. Persisting nutrient deficiencies once gluten has been removed from the diet may be due to:
a. slow or incomplete healing of the small intestine.
b. the failure to eat foods rich in needed nutrients.
c. eating too much fiber with meals.
d. All of the above

Oats: A Caution
Some people with celiac disease experience symptoms and damage from pure oats. No test is commercially available to identify whether a person with celiac disease can tolerate oats, and symptoms are unreliable indicators of damage. Therefore, caution is advised when considering using pure oats.2

Examples of Health Problems in Celiac Disease3
Abdominal pain/bloating
Acid reflux
Anemia                                    
Arthritis
Autoimmune disease
Behavior disorders
Cancers
Chronic constipation
Chronic diarrhea           
Chronic fatigue
Dental enamel defects
Depression
Dermatitis herpetiformis
Diabetes
Heart disease   
Infertility
Insomnia
Irritability
Irritable bowel syndrome
Migraine
Neuropathies   
Osteoporosis   
Swelling
Unexplained weight gain/loss