GO GLUTEN-FREE Diets for Athletes and Active People by Margaret M. Harris, Ph.D., M.S., H.C. and Nanna Meyer, Ph.D., R.D., C.S.S.D., FACSM LEARNING OBJECTIVES • To understand the difference between celiac disease, gluten intolerance, and wheat sensitivity CELIAC DISEASE • To gain knowledge on diagnosis and management for varying levels of gluten intolerance • To gain knowledge on special issues when following a glutenfree diet, especially for active individuals Key words: Celiac Disease, Gluten Intolerance, Wheat, Ingredients, Carbohydrate THE GLUTEN-FREE FAD B y the end of 2011, an estimated $1.3 billion of gluten-free (GF) products had been purchased and produced. That’s an increase of 110% during the last 10 years, making the GF market one of the fastest growing markets (8). Walking through a store, the amount of sections promoting GF products is apparent. More restaurants and bakeries also are offering GF sections on their menus. The question always arises, however, whether the GF ideology is a fad, a result of true increasing food allergies, or a meritorious claim to healthier living. This is an important and pertinent question for the athlete. Many athletes are turning to GF diets under the idea that the diet provides health benefits and improved athletic performance. WHAT IS GLUTEN? Gluten is a protein that is found in wheat and other grains, such as barley, kamut, and spelt. Gluten has an elastic and gluelike capacity that makes grain products chewy. Commonly consumed gluten-containing products include pasta, bread, pastries, croutons, and cereals. Gluten is a hidden ingredient in many food products on the market: soy sauce, pie fillings, foods that contain ‘‘hydrolyzed protein,’’ some canned foods, deli meats, 22 beer, foods with sugar alcohols, sauces, and fast food. Gluten also may be found in preservatives, breading, and thickening agents. For some people, eating GF is a choice. But for a growing number of people, eating GF is necessary. People for whom a GF diet is beneficial and even life-saving are those with celiac disease (CD), gluten intolerance (GI), and wheat allergy (WA). Although these types of sensitivities to gluten are different in their origins, they are treated the same way: a GF diet. CD is not a food allergy. It is an autoimmune disorder in which the small intestine is hypersensitive to gluten. The digestive tract contains tiny hairlike projections called villi, where food is absorbed. These villi are destroyed in people with unmanaged CD. When the villi are not functioning properly, nutrient deficiencies will result because carbohydrates, fats, proteins, vitamins, and minerals, and even water in some instances, cannot be absorbed. In the athlete, the malabsorption also leads to decreased exercise performance (5,8). Some symptoms of CD include diarrhea or constipation (or a combination of both), intestinal cramping, gas, pale fatty runny stools (steatorrhea), anemia, weight gain, or unexplained weight loss with an increased appetite. Weight gain has been a puzzling yet new observation. Once labeled a malabsorption syndrome, the hallmark of CD has been wasting. Today, many people with CD are normal weight or overweight. CD affects not only the gut but also many other parts of the body and organs. The primary symptoms are listed in Table 1. Some people do not exhibit any symptoms until CD has become severe. Individuals often have CD for more than a decade before a diagnosis is made. True CD is a life-threatening condition and has been associated with many other disorders, such as leaky gut syndrome, hypothyroidism, type I diabetes, and other autoimmune diseases. ACSM’s HEALTH & FITNESS JOURNALA | www.acsm-healthfitness.org Copyright © 2013 American College of Sports Medicine. Unauthorized reproduction of this article is prohibited. VOL. 17/ NO. 1 Once considered a rare disease, the prevalence of CD has increased dramatically during the last 100 years. Today, it is thought to affect 1% of the population (2). This disease is underdiagnosed, and this estimate is thought to be grossly underestimated. Because this disease is genetically based, first-degree relatives will have an increased risk of also being diagnosed with CD, as high as 1 in 22 (2). Diagnosis is based on a blood test. However, false-negatives are an issue. A combination of blood tests (i.e., testing for antibodies and tissue damage), genetic markers, and history is ideal. A tissue biopsy of the small intestine is the ultimate standard for CD diagnosis. Because the only treatment available for CD is a strict GF diet, a person may want to try a GF diet even if his or her test is negative. People who test negative at first may test positive years later. When undergoing testing, individuals who have been following a GF diet will yield negative results on blood tests and biopsies because the body will have had a chance to heal. For accurate testing for CD, the patient needs to eat gluten for several weeks before the test. GLUTEN INTOLERANCE GI is very similar to CD. People with GI suffer similarly to people with CD but do not test positive for CD. Unlike CD, where the person can have no gluten in his or her diet from any source, people with GI exhibit a range of gluten sensitivity. Some may be able to eat small amounts of gluten until they reach a threshold, whereas others cannot tolerate any gluten. About 5% to 10% of the population may have some degree of GI, but higher estimates have also been reported (3). The reason for this dramatic rise (in both GI and CD) is unknown. Marion Nestle, author of Food Politics, claims that the higher prevalence is caused by more awareness of the disorder (hence, better diagnosis) (7). Unfortunately, blood tests cannot be routinely used to diagnose GI. Individuals with GI may exhibit more than 100 documented symptoms associated with GI, and people do not react similarly. Some commonly seen symptoms that improve with a GF diet are included in Table 1. Gluten ataxia, one of the symptoms, is a relatively new concept that involves neurological dysfunction VOL. 17/ NO. 1 that exhibits itself as reduced coordination and muscle control (3). If an athlete has gluten ataxia, serious implications for sports performance may result. GI often can be subtle and will worsen with continued gluten consumption over time. Continued consumption of gluten with true gluten sensitivity will contribute to further deterioration of the body and lead to a multitude of degenerative symptoms (i.e., osteoporosis). Because gluten sensitivity is an autoimmune response, continued consumption of gluten can manifest other autoimmune disorders. The best way for people to determine if they are GI is to be evaluated and diagnosed by a gastrointestinal specialist and work with a registered dietitian on following an elimination diet. On this diet, a person completely eliminates all gluten and gluten-rich foods for several weeks and then slowly adds these foods back into the diet. Record keeping is essential to determine symptoms before and after the diet. Because this diet is quite difficult to follow, consultation with a registered dietitian is critical. The diagnosis of GI is still evolving and may also include testing for steatorrhea. WHEAT ALLERGY WA differs from GI and CD. People who have a WA have a systemic response to wheat similarly to how people with nut allergies may react. Symptoms of WAs are similar to symptoms of other allergies, namely, hives, swelling, and possibly stomach pain. CONCERNS FOR THE ATHLETE, FITNESS PROFESSIONAL, AND ACTIVE INDIVIDUAL Individuals who train strenuously and competitively need to plan their nutrition carefully for optimized athletic performance and decreased gastrointestinal symptoms. Quickly absorbing carbohydrates before, during, and after training are backed by years of scientific research to improve such performance (4). Many athletes are turning to the GF diet to reduce gastrointestinal symptoms. Anecdotal claims suggest that the GF diet also will TABLE 1: Some Common Symptoms of Celiac Disease and Gluten Intolerance Abdominal bloating, gas, pain, cramping, or distension Unexplained weight loss/obesity Chronic diarrhea (can be accompanied by constipation) Pale, foul-smelling stool (steatorrhea) Anemia or other nutritional deficiencies Irritability, anxiety, depression, fatigue Bone or joint pain Hypoglycemia Muscle cramps, mouth sores, hair loss Missed menstrual periods Gluten ataxia Tingling or numbness in extremities Bone density loss (osteoporosis/osteopenia) Extremely itchy rash ACSM’s HEALTH & FITNESS JOURNALA Copyright © 2013 American College of Sports Medicine. Unauthorized reproduction of this article is prohibited. 23 Go Gluten-Free amounts of gluten. However, pasta and breads made from GF courses (i.e., rice, corn, quinoa) are available. Many GF products are not enriched with vitamins and minerals as are conventional products. People on GF diets may be at risk for micronutrient deficiencies, although GF flours are naturally nutrient dense. Athletes may find it difficult to adhere to a strict GF diet, filled with wholesome GF grains, fruits, and vegetables, especially when traveling. In addition, these foods are high in fiber that may pose additional gastrointestinal issues during training. Athletes and active individuals need more assistance when planning a GF diet at home or on the road to prevent nutrient deficiencies. Supplementation may need to be a consideration. reduce inflammation and improve performance. Unfortunately, these claims are testimonial based with limited research to support them. Athletes who improve performance with a GF diet may have undiagnosed CD or GI. They may improve their nutrient intake by switching to a GF diet, or they may lose weight, and thus feel and perform better. Therefore, a GF diet would naturally improve performance. More research is needed to prove or disprove this theory for people without CD or GI. Although a low body mass index is considered to be a hallmark of CD, obesity in CD patients is higher than was suspected. For example, one study found that almost one half of CD patients are overweight at the time of diagnosis (9). Some preliminary research suggests that overweight people with CD lose weight when placed on a GF diet (1). Overcompensation for intestinal malabsorption is one explanation for this phenomenon. When the intestinal tract is damaged, nutrients cannot be absorbed, resulting in micronutrient deficiencies, which may drive food cravings (6). The issues that arise from consuming a GF diet, however, also need to be addressed. GF diets are significantly more expensive than non-GF diets. Developing a healthy GF pantry can be quite challenging. Many GF products are energy dense but not necessarily nutrient dense. For example, in a regular box of crackers, the primary ingredient used is white flour. In GF crackers, the flours may include potato starch, rice flour, or other GF flours. These flours are processed and are more energy than nutrient dense. These products might be a good option during training, when rapidly absorbing carbohydrates are necessary. During the off season, these foods can become a source of excess energy. The type(s) of GF flour will determine the amount of fiber in the product. Athletes should check labels and focus on lower fiber options before, during, and after exercise training. GF diets do not mean carbohydrate-free diets, a concept commonly confused. Whether an athlete is on a GF diet by choice or necessity, the proper amount of carbohydrates is needed to fuel training and competition. Many GF products available on the market consist of rapidly absorbed carbohydrates. Pastas and breads, typically recommended for intense training, contain high 24 DINING OUT GLUTEN-FREE Athletes and active individuals may travel a great deal for competition or work. These individuals should be familiar with foods allowed on a GF diet. Table 2 summarizes foods to avoid, foods to carefully consider, and foods to consume when following a GF diet. Fortunately, many restaurants provide GF options. Extreme care should be noted because these menu items may not always be GF. Athletes and active individuals should be aware of hidden sources of gluten (i.e., soy sauce). Finally, in a restaurant, cross contamination is always a concern. The following points should be considered when dining: • If the menu contains many breaded or fried foods, cross contamination may result. The cooks may not realize that cooking GF foods on equipment with gluten-rich foods will contaminate the food. For example, GF foods cooked in the same oven or grill station where gluten-rich foods were cooked could become contaminated. For example, is the chicken prepared on the same grill where the hamburger bun is toasted? • Customers should call the restaurant and ask about the knowledge of the chef and kitchen staff with GF. Customers should be provided with a detailed answer about how the kitchen is prepared for GF recipes rather than general statements. If a consumer calls the restaurant and is not reassured with specifics about how GF menus are prepared, he or she should choose an alternative dining establishment. Choosing a restaurant that obtains foods from sustainable sources such as local/organic farms can help a customer feel safer when ordering GF foods. Conventional meat and farmed fish may have been fed grain (and gluten)-filled food, which may be problematic for some individuals. The Gluten-Free Restaurant Awareness Program is a network that provides a resource of restaurants that serve GF menus following consistent guidelines (http://glutenfreerestaurants.org/). These tips, for a person with a true allergy, GI, or CD, may prevent extreme discomfort or a trip to the hospital. • ACSM’s HEALTH & FITNESS JOURNALA | www.acsm-healthfitness.org Copyright © 2013 American College of Sports Medicine. Unauthorized reproduction of this article is prohibited. VOL. 17/ NO. 1 TABLE 2: Foods and Ingredients of Concern to a GF Diet Avoid Be Careful* You Can Safely Consume Gluten-rich ingredients Foods with possible hidden gluten (avoid unless labeled ‘‘gluten-free’’) No gluten Semolina wheat (pasta, bread, pastries) Oatsy Buckwheat z Spelt Fried foods (i.e., french fries) Rice (brown or white) Kamut Beer, malt beverages, hard lemonade, and coolers Quinoa Barley Breads Potato starch Rye Pastries Tapioca Bulgur Processed lunch meat Xanthan gum Farina Cereals Fruits Matzo meal Grains Vegetables Durum wheat Cookies Dairy (milk, cheese, etc.) Triticale Cakes Amaranth Croutons Arrowroot Gravies Corn Imitation meats/seafood Cornmeal Self-basting poultry GF flours (rice, potato, soy, corn, bean, teff, amaranth, millet, flax, arrowroot) Salad dressings Polenta Sauces (i.e., soy sauce) Hominy grits Canned soups Corn tortillas Medications` Wine Supplements` Distilled spirits Preservatives Cider Food additivesP Meat/seafood (unbreaded) k Products you handle Beans, seeds, nuts (unprocessed) SeasoningsP Coconut (milk, flour, flakes) *The safest way to ensure something is gluten-free is to choose simple whole foods and avoid boxed and processed foods. For example, tomato paste in tomato sauce may contain gluten agents but are not disclosed in ingredients. y Oats may be cross contaminated. Choose GF oats. If you have celiac disease, proceed with caution; some people still react to GF oats. z Spelt contains gluten, although less than other flours. People with gluten intolerance can experiment with spelt. People with wheat allergy and celiac disease should not eat spelt. ` May contain binding agents that contain gluten. P Ingredients include malt flavoring, food starch, hydrolyzed protein, hydrogenated vegetable protein, textured vegetable protein, monosodium glutamate, and so on. k Playdough, cosmetics, toothpaste, and so on. THE GF PANTRY Table 2 lists the foods that are GF (as well as those that are gluten-rich or have hidden gluten). Even when products should technically be GF, contamination with gluten may still be present (9). Individuals should choose simple wholesome foods or products with the ‘‘gluten-free’’ label. Checking ingredients, even of known products, may ensure that the product is truly GF. Because companies frequently change their formulations, something that was GF one year may not be GF the next. Oats are one product that may or may not be safe for individuals following a GF diet. Oats should not contain any gluten but are typically manufactured in plants where cross contamination occurs. If oatmeal is commonly purchased, individuals should look for a label that specifically states that VOL. 17/ NO. 1 the product was processed without cross contamination. The label should say ‘‘gluten-free’’ as opposed to ‘‘wheat-free.’’ Although this should be a safer alternative to people with GI, people with diagnosed CD still need to be careful. Because oats contain a protein that is similar in structure to gluten, some people with CD can still react to oats, even if they are certified GF. Spelt is an ancient grain that also contains gluten. However, spelt contains less gluten than other gluten-rich products and is nutritionally superior (more protein, fiber, and other nutrients) than wheat. Although a person with CD and WAs should not consume spelt, some people with lesser degrees of GI can safely experiment with this highly nutritious grain. Finally, to avoid cross contamination at home, a designated GF toaster is advised. When baking, GF foods should be baked ACSM’s HEALTH & FITNESS JOURNALA Copyright © 2013 American College of Sports Medicine. Unauthorized reproduction of this article is prohibited. 25 Go Gluten-Free before gluten-filled foods and then the oven should be cleaned. Everyday household chores also need to be carefully reviewed. For example, many dishwashing gloves are coated with wheatbased flour. The glue in stamps and envelopes also may contain gluten, as do many cosmetics, art supplies, sunscreens, lotions, soaps, detergents, medicines, and supplements. For a complete safe list, go to www.celiac.com. Health and fitness professionals may encounter clients who inquire about GF diets, their health effects, and whether eating GF may be a good choice for them. Many individuals experience GI symptoms but are not diagnosed with GI or CD. If symptomatic, the best referral a health and fitness professional may give to the client is to a medical professional to confirm a possible issue. However, the client may remain undiagnosed because of limitations of the tests. If the client is symptomatic but not diagnosed or is nonsymptomatic but is interested in trying a GF diet, it is important to inform them about the fact that GF diets also may be low in carbohydrate and can affect performance and recovery. In addition, GF diets may be low in micronutrients, resulting in deficiency. The best guidance for a serious exerciser with or without GI symptoms and interested in trying a GF diet would be provided by a nutrition professional (http://www.eartight.org/programs/rdfinder/). This is especially true if the client wants to learn more about GF grains, starchy vegetables (they are always GF), and other creative ways of integrating GF foods into a wholesome and athletically sound diet. References 1. Cheng J, Brar P, Lee A, Green P. Body mass index in celiac disease: Beneficial effect of a gluten-free diet. J Clin Gastroenterol. 2010;44(4):267Y71. 2. Fasano A, Berti I, Gerarduzzi T, et al. Prevalence of celiac disease in at-risk and not-at-risk groups in the United States: A large multicenter study. Arch Intern Med. 2003;163:286Y92. Recommended Readings and Resources Case S. Gluten-Free Diet: A Comprehensive Resource Guide. 4th ed. Canada: Case Nutrition Consulting; 2010. Celiac Disease Foundation [Internet]. Available from: http://celiac.org/. Food and Drug Administration [Internet]. 2011 [cited 2011 Aug 2]. A glimpse at ‘‘gluten-free’’ food labeling. Available from: http://www.fda.gov/ForConsumers/ConsumerUpdates/ucm265212.htm. Gluten Intolerance Group [Internet]. Available from: http://www.gluten.net/. Libonati J, Libonati C. Understanding celiac disease. Today’s Dietitian. 2009;11(6):50 [Internet] [cited 2009]. Available from: http:// www.todaysdietitian.com/newarchives/060109p50.shtml. National Institutes of Health [Internet]. Available from: http://www.celiac.nih.gov/. University of Chicago Disease Center [Internet]. Available from: http://www.celiacdisease.net/. University of Maryland Center for Celiac Disease [Internet]. Available from: http://medschool.umaryland.edu/celiac/. Disclosure: The authors declare no conflicts of interest and do not have any financial disclosures. Margaret M. Harris, Ph.D., M.S., H.C., is an assistant professor in the Sport Nutrition Program at the Health Sciences Department at the University of Colorado Colorado Springs. She has worked in community outreach for the last 10 years in the areas of obesity, general health and wellness, and food deserts. Nanna Meyer, Ph.D., R.D., C.S.S.D., is an assistant professor and graduate director of the Sport Nutrition Program in the Health Sciences Department at the University of Colorado Colorado Springs. She is a consultant to the U.S. Olympic Committee and sport dietitian of U.S. Speed Skating. 3. Hadjivassiliou M, Sanders DS, Grunewald RA, Woodroofe N, Boscolo S, Aeschlimann D. Gluten sensitivity: From gut to brain. Lancet Neurol. 2010;9:318Y30. 4. IOC Consensus Statement on Sport Nutrition. 2010 [cited on 2010 Oct 27]. Available from: http://www.olympic.org/Documents/Reports/ EN/CONSENSUS-FINAL-v8-en.pdf; http://www.olympic.org/ Documents/Reports/EN/en_report_1251.pdf. 5. Martin S. Against the grain: An overview of celiac disease. J Am Acad Nurse Pract. 2008;20:243Y50. 6. Murray JA, Watson T, Clearman B, Mitros F. Effect of a gluten-free diet on gastrointestinal symptoms in celiac disease. Am J Clin Nutr. 2004;79:663Y73. 7. Nestle M. Gluten intolerance becoming more becoming more commonplace. San Francisco Chronicle [Internet] 2009. Available from: http://www.sfgate.com/cgi-bin/article.cgi?f=/c/a/2009/05/29/ FDTT17NK4F.DTL. 8. NTDaily.com [Internet]. North Texas: NT Daily.com [cited 2011 Oct 25]. Available from: http://www.ntdaily.com/?p=59107. 9. Thompson T, Lee AR, Grace T. Gluten contamination of grains, seeds and flours: A pilot study. J Am Diet Assoc. 2010;110:937Y40. CONDENSED VERSION AND BOTTOM LINE The prevalence of celiac disease (CD) has increased significantly. Concomitantly, the gluten-free (GF) diet has become a popular approach to eating. A strict GF diet for athletes who have CD, wheat allergy, or gluten intolerance will improve health and may enhance performance. Athletes with suspect gastrointestinal symptoms, fatigue, or skin rash should seek evaluation and consult with a sport dietitian. Athletes with gluten restrictions (by choice or need) can train safely, confidently, and productively. However, research has not examined how GF diets may impact the athletic performance of athletes or active individuals who choose GF eating plans. 10. Venkatasubramani N, Telega G, Werlin SL. Obesity in pediatric celiac disease. J Pediatr Gastroenterol Nutr. 2010;51(3):295Y7. 26 ACSM’s HEALTH & FITNESS JOURNALA | www.acsm-healthfitness.org Copyright © 2013 American College of Sports Medicine. Unauthorized reproduction of this article is prohibited. VOL. 17/ NO. 1 RESEARCH Commentary Gluten-Free Diet: Imprudent Dietary Advice for the General Population? Glenn A. Gaesser, PhD; Siddhartha S. Angadi, PhD ARTICLE INFORMATION Article history: Accepted 29 May 2012 Keywords: Wheat Gluten Gut microbiota Fructan-type resistant starch Copyright © 2012 by the Academy of Nutrition and Dietetics. 2212-2672/$36.00 doi: 10.1016/j.jand.2012.06.009 G LUTEN-FREE DIETING HAS GAINED CONSIDERABLE popularity in the general population.1-3 Between 2004 and 2011 the market for gluten-free products grew at a compound annual growth rate of 28%, with annual sales expected to reach approximately $2.6 billion in 2012.2 As of April 20, 2012, Amazon.com listed 4,765 entries for the topic “gluten-free.” A Google search at the same time for “gluten-free diet” produced more than 4.2 million results. The number-one reason consumers cite for buying gluten-free products is that they are perceived to be healthier than their gluten-containing counterparts.3 Endorsements from celebrities have undoubtedly contributed to the increased awareness of possible health benefits of gluten avoidance, including weight loss.4,5 Despite the health claims for gluten-free eating, there is no published experimental evidence to support such claims for the general population. In fact, there are data to suggest that gluten itself may provide some health benefits, and that gluten avoidance may not be justified for otherwise healthy individuals. Our primary purpose is to briefly describe this evidence and raise awareness of the potential pitfalls of adopting a gluten-free diet in persons without diagnosed gluten-related disorders. INDICATIONS FOR A GLUTEN-FREE DIET Gluten is a protein composite consisting of gliadins and glutenins, and is found in foods processed from wheat and related grains such as barley and rye. There is a spectrum of gluten-related disorders, including celiac disease, gluten sensitivity, and wheat allergy.1,2 Wheat allergy is an adverse immunologic reaction specific to wheat proteins.1,2 Prevalence of documented wheat allergy is quite low, estimated at only about 0.1% of individuals in Westernized countries.1 Because wheat allergy can be treated with wheat avoidance, a wheatfree diet may be more permissive than a strict gluten-free diet.1 Gluten sensitivity (also referred to as nonceliac gluten 1330 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS intolerance), is characterized by a heightened immunologic reaction to gluten in genetically susceptible people.6 Clinical diagnosis is generally based on responses to a gluten-free diet.1 Common symptoms of gluten sensitivity, such as fatigue and headaches, and gastrointestinal distress, including gas, bloating, and diarrhea, frequently improve with the adoption of a gluten-free diet. The inherent subjectivity in diagnosis and resolution of these symptoms likely contributes to the popularity of gluten-free diets. Celiac disease is a complex autoimmune enteropathy that affects the small bowel after ingestion of gluten-containing grains, including wheat, rye, and barley, in genetically susceptible people.7 Estimated prevalence of celiac disease is approximately 1%.8,9 The disease can manifest itself in a range of clinical presentations, including malabsorption syndrome and a spectrum of symptoms affecting multiple target organs.10 A strict gluten-free diet is an established remedy for individuals with celiac disease because it has been shown to lower incidence of related diseases, such as gastrointestinal cancers.7-9,11 Lifelong adherence to a strict gluten-free diet, devoid of proteins from wheat, rye, barley, and related cereals, remains the gold standard of treatment in celiac disease.7-9 There are some data to suggest that following a gluten-free diet may ameliorate gastrointestinal and/or systemic symptoms in individuals with systemic lupus erythematosus, dermatitis herpetiformis, irritable bowel syndrome, rheumatoid arthritis, type 1 diabetes, thyroiditis, and psoriasis.12,13 Gluten-free diets have also been used by patients with autism spectrum disorders (ASD).2,14 However, there are no definitive data to support the use of gluten-free diets in ASD,15 and the American Academy of Pediatrics does not support the use of gluten-free diets as a primary treatment for individuals with ASD.16 Apart from the demonstrated effectiveness of a gluten-free diet for treating the spectrum of gluten-related disorders and the conditions mentioned above, evidence-based research supporting the merits of a gluten-free diet as a healthier option for the general population is lacking. GLUTEN-FREE DIET AND WEIGHT LOSS: WHERE IS THE EVIDENCE? Despite the growing popularity of gluten-free diets and celebrity endorsements of the merits of a gluten-free diet for weight loss,4,5 there are no published reports showing that a gluten-free diet produces weight loss in persons without celiac disease or gluten sensitivity. There are a number of studies of patients with celiac disease that reported weight change as an outcome measure following a gluten-free diet.17-19 © 2012 by the Academy of Nutrition and Dietetics. RESEARCH Strict adherence to a gluten-free diet in celiac disease generally improves body mass index (BMI) status.17 However, normalization of BMI while following a gluten-free diet is not always observed. In a study of 369 adults with celiac disease who followed a gluten-free diet for an average of 2.8 years, 22 of 81 (27%) initially overweight or obese patients gained weight.17 In a study of 371 adults with celiac disease who followed a gluten-free diet for 2 years, 55 of 67 (82%) initially overweight patients gained weight.18 Among 149 children with celiac disease who followed a gluten-free diet for at least 12 months, the percentage of overweight children almost doubled (11% to 21%).19 These reports indicate that for a significant percentage of overweight or obese patients with celiac disease, body weight may actually increase on a gluten-free diet. This may be due in part to enhanced absorption of nutrients associated with healing of intestinal lining while following a gluten-free diet. Whether weight gain would be observed in persons without celiac disease or gluten sensitivity remains to be established. In this regard it is important to note that gluten-free does not necessarily mean low-energy, and some gluten-free products actually have a greater energy value than corresponding gluten-containing foods.3 Furthermore, a gluten-free diet may be deficient in whole grains and fiber,3 both of which have been shown to be inversely associated with BMI.20 WHEAT AND GASTROINTESTINAL HEALTH Naturally occurring fructan-type resistant starches in wheat, such as oligofructose and inulin, are beneficial for creating a healthy composition of gut bacteria,21-28 and these diet– microbe interactions in the colon may protect the gut from some cancers, inflammatory conditions, and cardiovascular disease.27,28 Wheat is the most widely consumed grain in the United States, and contributes approximately 70% to 78% of the oligofructose and inulin in typical North American diets.29,30 Wheat-derived nondigestible carbohydrates have been reported to decrease postprandial glycemia and insulinemia, reduce fasting triglycerides, and reduce body weight.21 Oligofructose has been shown to improve immune status, lipid metabolism, and vitamin and mineral absorption.25 By removing the major source (wheat) of fructan-type resistant starches in American diets, strict adherence to a gluten-free diet could have adverse consequences. In fact, recent evidence suggests that a gluten-free diet may lead to reductions in beneficial gut bacteria.31 Ten healthy subjects followed a gluten-free diet for 1 month by replacing gluten-containing foods with equivalent products certified as gluten-free.31 The gluten-free diet significantly reduced a number of beneficial bacteria in fecal samples of the subjects, including Bifidobacterium, Lactobacillus, Clostridium lituseburense, and Faecalibacterium prausnitzii, and increased levels of pathogenic Enterobacteriaceae and Escherichia coli. Immunostimulatory properties of fecal samples were also reduced after 1 month following a gluten-free diet. For example, the gluten-free diet reduced production of the potent neutrophil chemoattractant tumor necrosis-␣. Three-day food diaries (2 weekdays and 1 weekend day) at the beginning and end of the 1-month diet period indicated that total energy and macronutrient intake were not changed, with the exception of a lower polysaccharide intake while following the gluten-free diet. A reduction in polysaccharide intake on a gluSeptember 2012 Volume 112 Number 9 ten-free diet is not unexpected.32 Thus, a gluten-free diet produced potentially adverse changes in gut health as a result of reduced intake of naturally occurring fructans in wheat products that have a prebiotic action. By contrast, increasing whole-grain wheat intake has been reported to increase beneficial gut bacteria.33 In a doubleblind, randomized, crossover study consisting of two 3-week dietary periods with a 2-week washout in between, 31 healthy women and men added to their diet either 48 g/day 100% whole-grain wheat breakfast cereal or 48 g/day wheatbran cereal. Fecal samples were collected before and after the 3-week dietary period. After 3 weeks following the diet supplemented with 48 g/day 100% whole-grain wheat breakfast cereal, numbers of fecal Bifidobacterium were increased by approximately 10%. Addition of wheat bran to subjects’ habitual diets had no effect. Both 100% whole-grain wheat and wheat-bran conditions increased the numbers of lactobacilli in fecal samples, but the 7.4% increase after the 100% wholegrain wheat condition was significantly greater than the 5.0% increase observed after the wheat– bran condition. The results indicate a prebiotic effect of whole-grain wheat breakfast cereal. It has been proposed that one of the mechanisms by which whole-grain foods confer health benefits is via their beneficial effect on gut bacteria.21-28 These findings may help explain the well-established inverse relationship between whole-grain food intake and risk of cardiovascular diseases.25,26 GLUTEN AND HEALTH Gluten itself may actually be beneficial to the diets of individuals with dyslipidemia without celiac disease or gluten sensitivity. In 24 adults with hyperlipdemia, increased consumption of wheat gluten for 2 weeks on a weight-maintenance diet reduced serum triglycerides by 13%.34 In this randomized crossover study, subjects consumed diets that differed with respect to gluten, wheat fiber, and bran content. The higher gluten content of the diet was achieved by having subjects consume bread that contained 53.1% protein. This increased gluten intake by 60 g/day, which accounted for 10% of total energy. High levels of wheat fiber and bran did not reduce triglyceride levels when gluten levels were the same in each diet. Only under the high-gluten condition, regardless of wheat fiber content, were triglyceride levels reduced. Therefore, it appeared that the reduction in serum triglyceride levels was attributable to the gluten itself rather than the wheat fiber. In a randomized crossover study of men and women with hyperlipidemia,35 subjects consumed either a control diet or a diet in which 11% of the carbohydrate in the control diet was replaced with vegetable protein (as wheat gluten) for 1 month. This resulted in a 78 g/day increase in gluten intake. Total energy, dietary fiber, and fat intake were the same during each diet period. Increasing daily gluten intake for 1 month reduced serum triglycerides by 19.2%, uric acid by 12.7%, and creatinine by 2.5%. In addition, low-density lipoprotein oxidation was reduced by 10.6% in the high-gluten diet. The authors concluded that high intake of vegetable protein in the form of added wheat gluten could have beneficial effects on triglyceride levels and oxidized low-density lipoprotein similar to those of monounsaturated fat and soy protein. In addition to the potential benefits of gluten for improving blood lipid levels,34,35 gluten may play a role in blood pressure JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 1331 RESEARCH control. For example, wheat gliadin hydrolysates have been reported to inhibit angiotensin I-converting enzyme (ACE).36 Thewissen and colleagues36 extracted gliadin from commercial wheat gluten and demonstrated that several of the resulting peptide fractions from the gliadin hydrolysates exhibited ACE-inhibitory activity. Because ACE converts angiotensin I into angiotensin II (vasoconstrictor) and degrades bradykinin (vasodilator), inhibition of ACE could facilitate reduction in blood pressure. Whole-grain consumption has been shown to reduce blood pressure,37 with wheat itself having a demonstrated effect.38 Although the dietary fiber component of whole grains is thought to play a role,39 it is also possible that gluten, via one of its constituent proteins gliadin, may contribute to the blood-pressure–lowering effect of whole grains.36 Gluten may also boost the immune system in humans. This may be due in part to the very high glutamine content of gluten (⬃40% of total amino acids). Glutamine supplementation, for example, has been reported to reduce incidence of infectious complications in patients following surgery.40 In a small study of nine healthy volunteers, five subjects received 3 g/day wheat gluten hydrolysate for 6 days (41). After 6 days, natural killer cell activity was increased significantly (by approximately 6% to 57%; P⬍0.05) in all five subjects who received the wheat gluten hydrolysate. No change was observed in the four control subjects.41 There were no reported side effects. An increase in natural killer cell activity could be expected to enhance immune monitoring against tumor development and viral infections.42 Epidemiologic evidence supports a protective role for whole-grain consumption to reduce cancer risk,43 with specific effects attributable to wheat.44,45 CONCLUSIONS Gluten-free diets are clearly indicated for patients with celiac disease or for persons with gluten sensitivity, and may be beneficial for individuals with other chronic autoimmune disease conditions such as psoriasis, rheumatoid arthritis, and type 1 diabetes.12,13 With the substantial growth in the gluten-free products market,2 a greater number of food choices are now available to individuals for whom gluten avoidance is essential. There are many gluten-free grains available to help consumers obtain the benefits of whole grains and overcome some of the nutritional deficiencies (eg, inadequate intakes of thiamin, riboflavin, niacin, folate, and iron) reported to be associated with gluten-free diets.9,46 A gluten-free diet can be a well-balanced diet if care is taken in choosing whole-grain products, including more legumes, and selecting foods with lower energy density. This does not imply that a gluten-free diet, per se, is a healthier diet. Despite numerous health claims and the exploding popularity of gluten-free products, there are no published data to support a weight loss claim for a gluten-free diet.3 Results of several studies of patients with celiac disease suggest that a gluten-free diet may actually worsen BMI status in some overweight and obese individuals. Gluten-free baked goods can be high in fat and total energy.9 Moreover, whole-grain intake is inversely associated with BMI, and wheat is the most widely consumed grain in America. Thus, going gluten-free for purposes of weight loss may have unintended consequences. Randomized-control trials are necessary to establish the effect of a gluten-free diet on weight loss in overweight or 1332 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS obese individuals for whom a gluten-free diet is not medically indicated. Gluten-rich grains, especially wheat, may have health benefits attributable to naturally occurring fructan-type resistant starches as well as gluten itself. By creating a healthy composition of colon bacteria, whole-grain wheat products may protect the gut from some cancers, inflammatory conditions, and cardiovascular disease. Gluten, and one of its component proteins gliadin, may contribute to blood pressure control and immune function. Because wheat is the main source of gluten in the American diet,29,30 these studies may help explain the consistent findings of health benefits of whole-grain consumption.25,26,43,44 There is no evidence to suggest that following a gluten-free diet has any significant benefits in the general population. Indeed, there is some evidence to suggest that a gluten-free diet may adversely affect gut health in those without celiac disease or gluten sensitivity.31 Additional research is needed to clarify the health effects of gluten, and potential consequences of avoiding gluten-containing grains. References 1. Piezak M. Celiac disease, wheat allergy, and gluten sensitivity: When gluten free is not a fad. JPEN J Parental Enterol Nutr. 2012;36(suppl 1):68S-75S. 2. Sapone A, Bai JC, Ciacci C, et al. Spectrum of gluten-related disorders: Consensus on new nomenclature and classification. BMC Med. 2012; 10:13. 3. Marcason W. Is there evidence to support the claim that a gluten-free diet should be used for weight loss? J Am Diet Assoc. 2011;111(11): 1786. 4. Hasselbeck E. The G-Free Diet: a Gluten-Free Survival Guide. New York, NY: Center Street Books; 2009. 5. Miley Cyrus: Gluten-free diet is responsible for weight loss. Huffington Post website. http://www.huffingtonpost.com/2012/04/10/ miley-cyrus-gluten-free-diet-weight-loss_n_1414641.html. Accessed April 20, 2012. 6. Hadjivassiliou M, Grunewald RA, Davies-Jones GAB. Gluten sensitivity as a neurological illness. J Neurol Neurosurg Psychiatry. 2002;72(5): 560-563. 7. Briani C, Samaroo D, Alardini A. Celiac disease: From gluten to autoimmunity. Autoimmunity Rev. 2008;7(8):644-650. 8. Catassi C, Fassano A. Celiac disease. Curr Opin Gastroenterol. 2008; 24(6):687-691. 9. Niewinski MM. Advances in celiac disease and gluten-free diet. J Am Diet Assoc. 2008;108(4):661-672. 10. Cascella NG, Kryszak D, Bhatti B, et al. Prevalence of celiac disease and gluten sensitivity in the United States Clinical Antipsychotic Trials of Intervention Effectiveness study population. Schizophrenia Bull. 2011;37(1):94-100. 11. Haines ML, Anderson RP, Gibson PR. Systematic review: The evidence base for long-term management of celiac disease. Aliment Pharmacol Ther. 2008;28(9):1042-1066. 12. Green PH. Mortality in celiac disease, intestinal inflammation, and gluten sensitivity. JAMA. 2009;302(11):1225-1226. 13. El-Chammas K, Danner E. Gluten-free diet in nonceliac disease. Nutr Clin Pract. 2011;26(3):294-299. 14. de Magistris L, Familiari V, Pascotto A, et al. Alterations of the intestinal barrier in patients with autism spectrum disorders and in their first-degree relatives. J Pediatr Gastroenterol Nutr. 2010;51(4):418424. 15. Mulloy A, Lang R, O’Reilly M, Sigafoos J, Lancioni G, Rispoli M. Gluten-free and casein-free diets in the treatment of autism spectrum disorders; a systematic review. Res Autism Spectrum Disord. 2010;4(3):328-339. 16. Buie T, Campbell DB, Fuchs GJ 3rd, et al. Evaluation, diagnosis, and treatment of gastrointestinal disorders in individuals with ASDs: A consensus report. Pediatrics. 2010;125 (suppl 1):S1-S18. September 2012 Volume 112 Number 9 RESEARCH blind, placebo-controlled, 2008;99(1):110-120. crossover study. Brit J Nutr. 17. Cheng J, Brar PS, Lee AR, Green PHR. Body mass index in celiac disease. Beneficial effect of a gluten-free diet. J Clin Gastroenterol. 2010;44(4): 267-271. 34. 18. Dickey W, Kearney N. Overweight in celiac disease: Prevalence, clinical characteristics, and effect of a gluten-free diet. Am J Gastroenterol. 2006;101(10):2356-2359. Jenkins DJA, Kendall CWC, Vuksan V, et al. Effect of wheat bran on serum lipids: Influence of particle size and wheat protein. J Am Coll Nutr. 1999;18(2):159-165. 35. 19. Valletta E, Fornaro M, Cipolli M, Conte S, Bissolo F, Danchielli C. Celiac disease and obesity: Need for nutritional follow-up after diagnosis. Eur J Clin Nutr. 2010;64(11):1371-1372. Jenkins DJA, Kendall CWC, Vidgen E, et al. High-protein diets in hyperlipidemia: Effect of wheat gluten on serum lipids, uric acid, and renal function. Am J Clin Nutr. 2001;74(1):57-63. 36. 20. Gaesser GA. Carbohydrate quantity and quality in relation to body mass index. J Am Diet Assoc. 2007;107(10):1768-1780. Thewissen BG, Pauly A, Celus I, Brijs K, Delcour JA. Inhibition of angiotensin I-converting enzyme by wheat gliadin hydrolysates. Food Chem. 2011;127(4):1653-1658. 21. Neyrinck AM, Delzene NM. Potential interest of gut microbial changes induced by nondigestible carbohydrates of wheat in the management of obesity and related disorders. Curr Opin Clin Nutr Metab Care. 2010;13(6):722-728. 37. Behall KM, Scholfield DJ, Hallfrisch J. Whole-grain diets reduce blood pressure in mildly hypercholesterolemic men and women. J Am Diet Assoc. 2006;106(9):1445-1449. 38. 22. Gibson GR. Prebiotics as gut microflora management tools. J Clin Gastroenterol. 2008;42(suppl 2):S75-S79. Tighe P, Duthie G, Vaughan N, et al. Effect of increased consumption of whole-grain foods on blood pressure and other cardiovascular risk markers in healthy middle-aged persons: A randomized controlled trial. Am J Clin Nutr. 2010;92(4):733-740. 23. Delzenne NM, Cani PD. Gut microbiota and the pathogenesis of insulin resistance. Curr Diab Rep. 2011;11(3):154-159. 39. 24. Jonnalagadda SS, Harnack L, Liu RH, et al. Putting the whole grain puzzle together: Health benefits associated with whole grains—Summary of American Society for Nutrition 2010 Satellite Symposium. J Nutr. 2011;141(5):1011S-1022S. Streppel MT, Arends LR, van’t Veer P, Grobbee DE, Geleijnse JM. Dietary fiber and blood pressure: A meta-analysis of randomized placebo-controlled trials. Arch Intern Med. 2005;165(2):150-156. 40. Novak F, Heyland DK, Avenall A, Drover JW, Su X. Glutamine supplementation in serious illness: A systematic review of the evidence. Crit Care Med. 2002;30(9):2022-2029. 25. Harris KA, Kris-Etherton PM. Effects of whole grains on coronary heart disease risk. Curr Atheroscler Rep. 2010;12(6):368-376. 41. 26. Slavin J. Why whole grains are protective: Biological mechanisms. Proc Nutr Soc. 2003;62(1):129-134. Horiguchi N, Horiguchi H, Suzuki Y. Effect of wheat gluten hydrolysate on the immune system in healthy human subjects. Biosci Biotechnol Biochem. 2005;69(12):2445-2449. 42. 27. Fava F, Gitau R, Lovegrove J, Tuohy KM. The gut microflora and lipid metabolism: Implications for human health. Curr Med Chem. 2006; 13(25):3005-3021. Herberman RB, Oltaldo JR. Natural killer cells: Their roles in defenses against disease. Science. 1981;214(4516):24-30. 43. Jacobs DR, Marquart L, Slavin J, Kushi LH. Whole-grain intake and cancer: An expanded review and meta-analysis. Nutr Cancer. 1998; 30(2):85-96. 44. Fardet A. New hypotheses for the health-protective mechanisms of whole-grain cereals: What is beyond fibre? Nutr Res Rev. 2010;23(1): 65-134. 45. Reddy BS, Hirose Y, Cohen LA, Simi B, Cooma I, Rao CV. Preventive potential of wheat bran fractions against experimental colon carcinogenesis: Implications for human colon cancer prevention. Cancer Res. 2000;60(17):4792-4797. 46. Case S. Gluten-Free Diet: A Comprehensive Resource Guide. Regina, Saskatchewan, Canada: Case Nutrition Consulting; 2006. 28. Rastall RA, Gibson GR, Gill HS, et al. Modulation of the microbial ecology of the human colon by probiotics, prebiotics and synbiotics to enhance human health: An overview of enabling science and potential applications. FEMS Microbiol Ecol. 2005;52(2):145-152. 29. van Loo J, Coussement P, de Leenheer L, Hoebregs H, Smits G. On the presence of inulin and oligofructose as natural ingredients in the Western diet. Crit Rev Food Sci Nutr. 1995;35(6):525-552. 30. Moshfegh AJ, Friday JE, Goldman JP, Ahuja JKC. Presence of inulin and oligofructose in the diets of Americans. J Nutr. 1999;129(7 suppl): 1407S-1411S. 31. De Palma G, Nadal I, Collado MC, Sanz Y. Effects of a gluten-free diet on gut microbiota and immune function in healthy adult human subjects. Br J Nutr. 2009;102(8):1154-1160. 32. Kinsey L, Burden ST, Bannerman E. A dietary survey to determine if patients with coeliac disease are meeting current healthy guidelines and how their diet compares to that of the British general population. Eur J Clin Nutr. 2008;62(11):1333-1342. 33. Costabile A, Klinder A, Fava F, et al. Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: A double- AUTHOR INFORMATION G. A. Gaesser is a professor, Exercise and Wellness Program, Healthy Lifestyles Research Center, School of Nutrition and Health Promotion, Arizona State University, Phoenix. S. S. Angadi is a postdoctoral scholar, Exercise and Metabolic Disease Research Laboratory, Translational Sciences Section, UCLA School of Nursing, Los Angeles, CA. Address correspondence to: Glenn A. Gaesser, PhD, Healthy Lifestyles Research Center, School of Nutrition and Health Promotion, Arizona State University, 500 N 3rd St, Phoenix, AZ 85004. E-mail: [email protected] STATEMENT OF POTENTIAL CONFLICT OF INTEREST G. A. Gaesser is chairman of the Grain Foods Foundation Scientific Advisory Board. FUNDING/SUPPORT Preparation of this article was supported in part by a grant from the Grain Foods Foundation. September 2012 Volume 112 Number 9 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 1333
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