Social and Behavioral Characteristics of Individuals with Celiac Disease. A Thesis. Presented in Partial Fulfillment of the Requirements for

Transcription

1 Social and Behavioral Characteristics of Individuals with Celiac Disease A Thesis Presented in Partial Fulfillment of the Requirements for the Degree of Master of Science in the Graduate School of The Ohio State University By Alexandra M. Borsuk, B.S. Graduate Program in Health and Rehabilitation Sciences The Ohio State University 2013 Master s Examination Committee: Dr. Christopher A. Taylor, Advisor Dr. Marcia Nahikian-Nelms Mary Kay Sharrett, MS, RD, CNSD

2 Copyright by Alexandra M. Borsuk 2013

3 Abstract We sought to describe the weight status, weight change, food security, and consumer behaviors of individuals serologically positive for CD. There is a need for more research to describe the profile of participants with CD, identify their weight status and food procurement and preparation habits. Recent research points to the need for more evaluation of socioeconomic factors as related to celiac disease. This study included persons aged 6 years or older who participated in the National Health and Nutrition Examination Survey (NHANES) from Serum samples from all participants were tested for immunoglobulin A (IgA) tissue transglutaminase antibodies and, if findings were abnormal, also for IgA endomysial antibodies. Weight and waist circumference were collected. Information about demographics, food security, weight status, and consumer behaviors were obtained by home interview. Two-thirds of the sample was found to be overweight or obese. Their weight status has remained stable within the past ten years. The majority of the sample was non- Hispanic white. Fifteen percent of the sample was found to be food insecure. Meal planning and preparation was shared with a spouse in about 50% of the sample. Individuals that are serologically positive for CD tend to be overweight or obese. They tend to eat out a few times a week and seem to prefer convenient foods for mealtime. Barriers such as food access, food affordability, access to medical testing, and issues of cross contamination can be a problem for this population. ii

4 Dedication Dedicated to my Nana and Papa, Theresa and Joe Kocsis. Thank you so much for your love and interest in everything that I do. iii

5 Acknowledgements First and foremost, I would like to acknowledge Dr. Chris Taylor for his patience, guidance, and dedication throughout the past two years. He played a vital role in the development of my research for which I am very thankful. I would also like to thank my other committee members; Dr. Marcia Nelms and Mary Kay Sharrett, for their flexibility, input, and knowledge, and support they have provided me throughout this project. This thesis would not have been possible without my committee s invaluable knowledge and support. Lastly, I would like to thank my parents for their unconditional support and immense amount of love they have given me during the pursuit of my Master s Degree, and throughout my life. Your hard work has helped make it possible for me to attain such a level of education. And to Matt - your uplifting words and loving heart have been a great support throughout this endeavor I cannot thank you enough. iv

6 Vita June 2007 June 2011 April 2013 Saint Joseph Academy Cleveland, Ohio B.S. Applied Nutrition, Ohio University Athens, Ohio Graduate Program in Clinical Nutrition, School of Health and Rehabilitation Sciences, The Ohio State University Columbus, Ohio Major Field: Clinical Nutrition Medical Dietetics Field of Study v

7 Table of Contents Abstract... ii Dedication... iii Acknowledgements... iv Vita...v List of Tables... viii Chapters: Introduction...1 a. Background and Significance...1 b. Purpose of Research Study...2 c. List of Definitions...3 d. List of Abbreviations Review of Literature...6 a. Overview of Celiac Disease...6 b. Diagnostics...9 c. Gluten-Free Diet...10 d. Treatment of Celiac Disease...11 e. Health Consequences of Celiac Disease...13 f. Compliance Issues and Barriers to Treatment...16 g. Cost and Availability Issues...17 h. Quality of Life...19 i. Conclusion Methodology...21 a. Research Overview...21 b. Research Questions...21 c. NHANES Overview...21 d. Subjects...22 e. Data Collection and Preparation Results and Discussion...26 a. Results...26 b. Discussion...31 c. Conclusion...36 vi

8 5. Social and Behavioral Characteristics of Individuals with Celiac Disease...38 a. Abstract...38 b. Introduction...39 c. Materials and Methods...41 d. Results and Discussion...43 References Cited...50 vii

9 List of Tables Table Page Table 1 Demographic Characteristics of Serologically Positive Participants...27 Table 2 Weight, Behavioral, and Socioeconomic Characteristics of Serologically Positive Participants...28 Table 3 Weight Characteristics of Serologically Positive Participants...30 Table 4 Age and Food Preparation Habits of Serologically Positive Participants...31 viii

10 Chapter 1: Introduction Background and Significance Celiac disease (CD) is an autoimmune disease which affects approximately 1% of the population in the United States 1-2. Gluten, a protein found in grains of wheat, barley, and rye, triggers an inflammatory attack of the small intestine 3-5. Oats, while not inherently gluten-containing, are considered unsafe for consumption when crosscontaminated with wheat and other gluten sources during harvesting and processing. Strict, lifetime adherence to a gluten-free diet is the only acceptable treatment for the disease. Eating gluten found in the grains of wheat, rye, barley, and hybrid wheat varieties, as well as food products containing these grains, can cause serious damage to the small intestine by triggering an autoimmune reaction. Gluten is hidden in many products such as seasonings, sauces, marinades and dressings 6. Issues with labeling can make compliance with the gluten-free diet difficult. Untreated celiac disease leads to a number of health consequences, such as malabsorption, weight loss, and chronic complications such as cancer, osteoporosis, and osteomalacia. Classic symptoms of CD include diarrhea, abdominal pain, constipation, weight loss, and anemia 3,7. Most symptoms that occur with CD are caused by the malabsorption of nutrients, vitamins, and minerals 6,8-9. Once a gluten-free diet is implemented and normal absorption is restored, the associated symptoms are resolved. 1

11 Compliance with a gluten-free diet can be difficult for a variety of reasons. Strict adherence is important because gluten re-exposure results in villous damage and an increased risk of cancer and osteoporosis and a return of malabsorptive symptoms Issues that make compliance difficult include poor food labeling, cost, and access to gluten-free foods. Gluten-free foods tend to be higher in price than their glutencontaining counterparts Additionally, gluten-free foods may have limited availability in restaurants and supermarkets Purpose of Research Study This study was developed to describe the weight status, weight change, food security, and consumer behaviors of individuals with CD. There is a need for more research to describe the profile of participants with CD, identify their weight status and food procurement and preparation habits. Additionally, recent research points to the need for more evaluation of socioeconomic factors as related to celiac disease. Research Questions 1. What is the weight status of individuals with CD? 2. What is the history of weight change in individuals with CD? 3. What is the food security status and food assistance program participation in individuals with CD? 4. What types of consumer behaviors do individuals with celiac disease have? 2

12 List of Definitions Autoimmune disease: A condition that occurs when the immune system mistakenly attacks and destroys its own healthy body tissue. Body Mass Index: An indicator of body weight status calculated as weight (kilograms) divided by height (meters) squared. Celiac disease: An autoimmune condition in which the small intestine is damaged upon the ingestion of gluten. Consumer behavior: The processes that individuals use to select, secure, and dispose of products and products to satisfy needs and the impact they have on the consumer and society. Cross-contamination: Indirect transfer of gluten from one place to another. Food assistance program: Programs which provide better access to food; The Supplemental Nutrition Assistance Program (SNAP) and The Special Supplemental Nutrition Program for Women, Infants, and Children (WIC). Food security: Having access to sufficient, safe, nutritious food to maintain a healthy and active life. Gluten: A storage protein found in wheat, rye, and barley. 3

13 Gluten-free diet: A diet in which the grains from wheat, rye, and barley are completely removed; the only acceptable treatment for celiac disease. Grain: Any small, hard seeds which are the edible fruit of certain grasses. NHANES: National Health and Nutrition Examination Survey; a program of studies designed to assess the health and nutritional status of children and adults in the United States. 4

14 List of Abbreviations BMI CAPI CBQ CD CDC DBQ ELISA EMA FDA IgA IgA anti-ttg IgA EMA MEC NHANES NCHS ttg US FSSM WC Body Mass Index Computer-Assisted Personal Interview Consumer Behavior Questionnaire Celiac Disease Centers for Disease Control and Prevention Dietary Behavior and Nutrition Questionnaire Enzyme-Linked Immunosorbent Assay Anti-Endomysium Antibody Food and Drug Administration Immunoglobulin A IGA Anti- Tissue Transglutaminase Antibody Endomyseal Antibody Assay Mobile Examination Center National Health and Nutrition Examination Survey National Center for Health Statistics Tissue Transglutaminase US Food Security Module Waist Circumference 5

15 Chapter 2: Review of the Literature Overview of Celiac Disease Celiac disease (CD) is a chronic, autoimmune disease affecting the small intestine primarily associated with malabsorption caused by an intolerance to gluten 3,5. This inflammatory response is caused by gluten, which is the protein peptide sequence that occurs in the alcohol soluble, prolamin fraction of wheat (gliadin), rye (secalin), and barley (hordein) 3-5. Gluten consumption in patients with CD causes atrophy of the villi in the small intestine, which are the small fingerlike projections that increase digestive and absorptive surface area 17. This decreased absorptive area leads to malabsorption of both macro- and micronutrients 8,18. The classical features of CD were first described by Samuel Gee, MDin 1887 as diarrhea, lassitude, and failure to thrive 19. He believed that the regulation of food was the main part of treatment for the disease. However, the relationship between the disease and wheat was first reported by Dickeafter World War II. He observed that the ingestion of cereal grains by children with CD was causing harmful effects 20. It was not until 1954 that Paulley provided the first accurate description of a celiac lesion. He examined full thickness biopsy specimens taken from a laparoscopy from a patient with CD and described broad, flat villi and a dense chronic lymphoephithelial inflammatory cell infiltrate in the small intestinal mucosa 1. 6

16 CD occurs in approximately 1% of the general population of the US 1,2. For reasons unknown, two to three times as many adult women have the disease than adult men 7. It occurs in 5-15% of the offspring and siblings of a person with CD 21. Also, in 70% of identical twin pairs, both twins were found to have the disease. Family members who have an autoimmune disease are at a 25% increased risk of having CD. However, since CD can be asymptomatic, most individuals are not diagnosed immediately; leading to about 7-10 undiagnosed or misdiagnosed individuals for each known CD patient 8,22. The disease itself can present in many ways, ranging from asymptomatic to symptomatic, and can be classified as atypical or latent. The term atypical CD is used for individuals who present with symptoms such as Immunoglobulin A (IgA)- nephropathy and an assortment of other neurological conditions 8. Those with atypical CD may also present with chronic fatigue, irritable bowel syndrome, infertility, miscarriage, pubertal delay, and dental enamel hypoplasia The term latent CD is classified by a late development of the disease and do not have intestinal damage despite a glutencontaining diet 26. Clinical presentation of classic, symptomatic CD varies greatly and depends on a patient s age, duration and extent of disease, and the presence of extraintestinal manifestations 27. Symptoms in children are usually associated with the introduction of cereal grains into the diet, usually around the age of six months 3. Symptoms depend on the age of onset. Classic symptoms include diarrhea, abdominal distention and failure to thrive 1,3,7, but may also include vomiting, irritability, anorexia, constipation, abdominal pain, and muscle wasting 3,7. In older children, the disease may present as anemia, rickets, 7

17 short stature, dental enamel damage, poor performance in school, or behavioral disturbances 3. CD in adulthood may be either adult-onset or silent without symptoms 3. Most symptoms presented are due to malabsorption of nutrients and vitamins, but clinical manifestations of the disease can differ significantly depending on each individual 6,8-9. Signs and symptoms depend partly on the amount and degree of the affected intestine 28. The iceberg model of the disease has been frequently applied to CD in that the tip of the iceberg represents patients with classic malabsorption, while the more atypical presentations represent the portion of the iceberg that is invisible, but much larger, below the waterline 29. The most common presenting symptoms in adults with CD are abdominal pain, chronic diarrhea, and iron-deficiency anemia 3,30. Other presenting symptoms may include constipation, weakness, short stature, flatus, and vomiting 7,18,23-25,31. The symptom of diarrhea is due to progression of the disease into the distal small bowel 1. Diarrhea in combination with steatorrhea, the presence of fat in the feces, is less common but indicates a more severe disease 3. Malabsorption can cause a variety of extraintestinal diseases, such as peripheral neuropathy, anemia, growth failure, bone pain, muscle cramps, night blindness, weight loss, edema, weakness, bleeding, and hematoma 6,8. Weight loss has historically been a classic symptom of celiac disease 7,14,18,23-25,31. However, the clinical picture of celiac disease has changed more recently, specifically, the proportion of patients who are rather over than underweight at diagnosis is increasing Few patients are underweight at diagnosis and a large minority is overweight 12. In a study by Ukkol et al, 39% of celiac disease patients were found to be overweight or obese, whereas, only a few were underweight 32. In another study by 8

18 Tucker et al, about half of CD patients were diagnosed with a BMI of 25 or over at the time of presentation 14. Diagnostics CD is commonly diagnosed in early childhood around the age of 2 years, and a second peak is found around the age of 40 years 28. There has also been a recent increase in diagnosis in females between the ages of 20 to 25 years old. However, many individuals with CD remain underdiagnosed 3. Fortunately, there have been new advances in both serologic and endoscopic testing which have significantly increased the detection and diagnosis of the disease 17. Because there is no single test that exists that can definitively diagnosis or exclude CD in every individual, serological testing is the first step in pursuing a diagnosis 6. Patients with low to moderate probability of CD should be screened using serological tests rather than be subjected to a small bowel biopsy 3. An intestinal biopsy is an invasive and expensive procedure and may not be justified in patients whom there is a low likelihood of the disease and serological testing is negative. These widely available tests are simple and minimally invasive, requiring only a blood test 3,34. The most sensitive and specific serological tests are the anti-endomysium antibody (EMA) and the IGA anti- tissue transglutaminase antibody (IGA anti-ttg) The IGA anti-ttg test has 90-95% specificity and 90-96% sensitivity, while the EMA test is the gold standard for serological testing, with 100% specificity. However, a positive serological test alone is not enough to make a diagnosis of CD. The benchmark diagnostic test for the disease is a small intestinal biopsy obtained during an upper endoscopy, a medical procedure used to visually examine the upper digestive system 3. During this procedure, multiple biopsies are taken from the second or 9

19 third part of the duodenum and analyzed for inflammation and evidence of damage or injury characteristic of gluten intolerance. A definitive diagnosis of CD can be made after a small intestinal biopsy confirms a flat jejunal mucosa with absence of normal intestinal villi 28. A complete diagnosis of CD relies on the clinical picture of the patient, serological markers for CD, characteristic findings of the small intestinal biopsy, and clinical improvement on a gluten-free diet. The average time it takes a person to be correctly diagnosed with CD is between six and ten years 22. A recent study investigated the long term outcome of undiagnosed CD and whether the prevalence of undiagnosed CD has changed during the past 50 years 29. The researchers concluded that during 45 years of follow up, undiagnosed CD was associated with nearly 4-fold increased risk of death. The prevalence of undiagnosed CD seems to have increased dramatically in the US during the past 50 years. Because of the large number of people undiagnosed and the related risk of mortality, proper and accurate diagnosis of CD is paramount. Gluten-Free Diet The gluten-free diet avoids consumption of gluten, found in wheat, rye, and barley. Gluten is also found in oats, but research suggests that the ingestion of oats is safe for most patients 10,36. However, oats can be considered unsafe when they have been contaminated with wheat or other gluten sources during harvesting, milling, and processing 8,37. Storsrud, Hulthen, and Lenner investigated the nutritional and symptomatic effects of including oats in the gluten-free diet. They examined food intake, gastrointestinal symptoms, blood samples, and body weight of twenty adult celiac patients who included large amounts of oats in their diets. They compared these 10

20 individuals to fifteen patients eating oats for 2 years and three eating oats for 6 months. It was found that oats improved the nutritional value of the gluten-free diet, had no negative effects on nutritional status, and were appreciated by the subjects 38. The use of oats increased patients intake of iron, dietary fiber, thiamin, and zinc. Individuals with CD may consume several types of gluten-free products in categories such as naturally-occurring gluten-free foods (fruits, vegetables, unprocessed meat, fish, poultry) and gluten-free substitute foods (pasta, bread, crackers, cereals) in which wheat flour is replaced by gluten-free flours 6,15. Naturally gluten-free grains, seeds, and starches allowed in the gluten-free diet include amaranth, arrowroot, buckwheat, corn, Indian rice grass, legumes, mesquite, millet, nuts, potato, quinoa, rice, sorghum, soy, tapioca, teff, and wild rice 37. Gluten can be found in many surprising products, such as seasonings, sauces, marinades, soy sauce, soups and salad dressings (32). Additionally, lack of knowledge about gluten can make label reading problematic. These factors can make issues with labeling and contamination difficult, making compliance with the gluten-free diet challenging. Treatment of Celiac Disease Medical nutrition therapy is the only accepted treatment for CD 37,39. Once a diagnosis of the disease has been firmly established, gluten has to be immediately withdrawn from the diet 8. This includes elimination of wheat, rye, and barley, and hybrid grains such as kamut and triticale 37. Complete, lifetime removal of gluten from the diet in a patient with CD will result in symptomatic, serologic and histological remission in the majority of patients after only a few weeks 3,25,33,40-41, but full normalization of the mucosa is less certain and can take several years 4,9,23,30, It may be obtainable, but often 11

21 requires longer than 12 months of strict adherence to a gluten-free diet 40,43. However, mucosal recovery does not occur in all patients with CD in whom complete clinical response is achieved 45. Rubio-Tapia, et al., aimed to estimate the rate of mucosal recovery after a gluten-free diet in a cohort of adults with CD and to assess the clinical implications of persistence mucosal damage after initiation of a gluten-free diet. Mucosal recovery was absent in a substantial portion of adults with CD after treatment with a gluten-free diet 44. Conversely, up to 95% of CD diagnosed during childhood may have complete intestinal mucosal recovery within 2 years after starting a gluten-free diet 46. Growth and development in children returned to normal with strict adherence to a gluten free diet and in adults, many disease complications are avoided and symptoms are resolved 6. Norstrom, et al., investigated the effect of a gluten-free diet on many factors, such as CD related symptoms and health care consumption 47. Using a questionnaire, members of the Swedish Society for Coeliacs answered questions regarding self-reported symptoms and health care consumption. Once a gluten-free diet was followed, CD patients experienced reduced symptoms and health care consumption. Treatment with a gluten-free diet for at least 12 months has resulted in increased body weight, body mass index, fat mass, bone mass, triceps skin fold thickness, and nutritional and biochemical status including iron absorption 2. While the gluten-free diet is still the only acceptable treatment for CD, recent investigations have explored alternative approaches for treatment, including the use of altered nonimmunogenic wheat variants, enzymatic degradation of gluten, tissue transglutaminase inhibitors, induction of tolerance, and peptides to restore integrity to intestinal tight junctions

22 Health Consequences of Celiac Disease Malabsorptive issues CD primarily affects the proximal small intestine, but can involve the entire small intestine in some individuals. This proximal location of CD often results in overt malabsorption of vitamins and minerals 6. Malabsorption of iron, folate, and calcium is common, as these nutrients are absorbed in the proximal small bowel. As the untreated disease progresses along the small intestine, malabsorption of carbohydrates, fat, fat soluble vitamins and other micronutrients occurs 25. Nutritional status of the newly diagnosed person with CD depends on the length of time the person has lived with untreated disease, extent of damage to the GI tract, and degree of malabsorption 6. At diagnosis, most individuals are found to be deficient in their intake of calories, protein, fiber, iron, calcium, vitamin D, magnesium, zinc, folate, niacin, vitamin B12, and riboflavin 13, Once a gluten-free diet is implemented, individuals with CD are still found to be deficient in iron, calcium, vitamin D, magnesium, folate, niacin, and vitamin B12. This is because many gluten-free products, such as bread and pasta, are not enriched with these nutrients like their traditional processed wheat counterparts. Gluten-free food products are typically lower in fiber, iron, folate, thiamin, riboflavin, and niacin 3,37. Those following a strict, long term gluten-free diet may still be at risk for folate, niacin, and vitamin B12 deficiencies due to the nutrient composition of the diet 51. In addition to macro- and micronutrient malabsorption, secondary lactose intolerance is also common among individuals with CD 3. Lactase is an enzyme that is needed to help digest lactose, the sugar found in milk. The body s lactase production is decreased due to the damaged villi in the small intestine, leading to both lactose 13

23 intolerance and a possible decreased calcium intake 52. For these reasons, temporary or long term vitamin and mineral supplementation may be necessary at the beginning of a gluten-free diet in subjects with CD to correct deficiencies and replenish nutrient stores 8,25,37. Because CD is a disease of malabsorption, most symptoms that occur are due to the malabsorption of nutrients, vitamins, and minerals 6,8-9. Malabsorption can cause many other complications, such as anemia, growth failure, weight loss, weakness, and bleeding. Symptoms of malabsorption include but are not limited to peripheral neuropathy, anemia, growth failure, bone pain, muscle cramps, night blindness, weight loss, edema, weakness, bleeding, and hematoma 6,8. Normal absorption is usually restored within a few months, although it may take up to two years in older adults. Once normal absorption is restored, the associated symptoms resolve. Weight status CD has variable effects on weight status among individuals. In some individuals, untreated CD may cause weight loss. This is due to malabsorption, in which the individual is unable to absorb vital nutrients from food, which leads to weight loss 7,18,23-25,31. Research has found that the BMI of underweight celiac patients increases after the initiation of a gluten-free diet, especially in those with strict adherence By eliminating gluten, the villi in the small intestine will properly absorb nutrients over time, leading to eventual weight gain and normalization. Similarly, one study found that the BMI of overweight and obese children with CD has been found to decrease toward healthy weight after a gluten-free diet has been initiated 54. However, in obese individuals, research has found that BMI decreases after the initiation of a gluten-free diet. For most 14

24 individuals, the gluten-free diet has been found to have a normalizing effect on weight status 32. Other research has found that the initiation of the gluten-free diet negatively impacts weight status for some individuals. Kabbani et al found that once celiac patients adopt a gluten-free diet, 15.8% of patients move from a normal or low BMI into an overweight BMI class, and 22% of patients overweight at diagnosis gain weight 53. There are reasons why individuals with CD may gain weight after diagnosis. Many gluten-free foods are processed and contain more fat and calories than their gluten-containing counterparts. Also, increased amounts of calories may have been necessary for consumption to prevent or slow weight loss caused by malabsorption 39. Once the intestine heals, fewer calories may be needed and caloric intake should be adjusted to control weight gain. The increase in weight in already overweight patients after gluten has been removed from the diet is a potential cause of morbidity and needs to be addressed 12. However, more research is needed in this area to determine the relationship of CD with weight status and weight change. Chronic complications Untreated CD increases risk for many chronic complications throughout the body, including malignancies, osteoporosis and osteomalacia. When CD remains undiagnosed for a long period of time or the gluten-free diet is not strictly followed, there is an increased risk of developing small intestinal cancer. The risk for developing lymphomas is much higher in celiac patients and is more likely to develop due to a compromised immune system. In addition, esophageal, pharyngeal, colorectal, and liver cancers have been shown to have a higher prevalence in this population 56. Malabsorption of vitamin D 15

25 and calcium can lead to the development of osteoporosis and osteomalacia 6,8-9. Supplementation of vitamin D and calcium may be necessary to address the nutritional needs in this population. Compliance Issues and Barriers to Treatment It can be exceedingly difficult to completely avoid gluten containing foods for a variety of reasons. Rates of adherence in adolescent populations vary from 56-83% 54, while rates in adults have been found to vary between 17-45% 11,57. Strict adherence to the gluten-free diet is important because gluten re-exposure results in villous damage and an increased risk of osteoporosis and malignancy Noncompliance can also cause other unwanted consequences, such as diarrhea, abdominal cramps, bloating, malabsorption and failure to thrive 10. Leffler used a nutritional assessment to determine adherence to the gluten-free diet in celiac participants and found that fewer than 50% of the participants had excellent gluten-free diet adherence 58. The low levels of adherence are troubling given the known morbidity and mortality associated with long-term untreated symptomatic CD and the lack of any other effective treatment 59. Rashid et al sought to characterize the adherence with a gluten-free diet in children with CD across Canada. Using a questionnaire, all members of the Canadian Celiac Association were surveyed with a questionnaire. Nearly all (95%) of the respondents reported strict adherence to a gluten-free diet. Although most of the respondents in this study reported to adjust well to their disease and diet, 10%-20% reported major disruptions in their lifestyle. Disruptions included anger about following the diet, traveling issues, avoidance of restaurants, and lack of stores with gluten-free foods 60. Additionally, the misunderstanding of gluten-containing ingredients on food 16

26 packages can lead to poor incidental compliance. Furthermore, gluten-free products may be difficult to find in in corner shops or smaller supermarkets, placing an even greater burden on individuals with CD of all incomes trying to address the therapy of their disease The high cost of these products adds an extra layer of burden to dietary compliance. Because the incidence and prevalence of CD has increased recently, the adherence and burden of the gluten-free diet needs to be addressed. However, there have been certain factors identified that may increase compliance of the gluten-free diet in individuals with CD. Leffler et al sought to determine the factors influencing gluten-free adherence in adults with CD. A questionnaire was given to 154 adults with CD who underwent a standardized gluten-free diet evaluation by a Registered Dietitian. It was found that understanding of the gluten-free diet, membership of a CD advocacy group, and perceived ability to maintain adherence despite travel or changes in mood or stress were significantly associated with improved adherence. Improving adherence reduces the risk for reoccurring symptoms of CD 58. Cost and Availability Issues CD can also pose a great economic burden for those following a gluten-free diet. Between the years of , the incidence and prevalence of CD doubled, resulting in an increased demand for gluten-free products 61. However, gluten-free foods are still two to three more times expensive than their regular gluten-containing counterparts 15. A study by Tucker et al found that gluten-free foods at two grocery stores were 180% more expensive than their standard counterparts 14.Whitaker et al found that half of the patients they surveyed with CD considered the diet to be more costly and for many, this was a considerable burden of the disease

27 Lee also sought to identify the economic burden of the gluten-free diet 15. A market basket of products identified by name brand, weight, or package size for both regular wheat-based products and gluten-free counterparts was developed. The differences in price between purchase venues, type of store, and region was analyzed. It was found that the availability of gluten-free products varied between the different venues, with regular grocery stores carrying only 6% of gluten-free products. It was also found that gluten-free products were more expensive than their wheat-based counterpart; bread and pasta were twice as expensive as their wheat-based counterpart. It was concluded that gluten-free foods have poor store availability and are more expensive than their gluten-containing counterparts. Other research has been done to determine the availability and cost of gluten-free foods 16. Singh and Whelan determined the availability and cost of 20 foods, surveyed at 30 different stores across five different categories. It was found that in general, there was limited availability of gluten-free foods with an average of 41% of foods available in a gluten-free version per store. It was also found that all gluten-free versions of wheat based foods were most costly than their standard counterparts. A Canadian study found that gluten-free foods at two grocery stores were 180% more expensive than their standard counterparts 14. In addition, the Canadian Celiac Association reported in 2003 that 85% of adults and 90% of children said that finding gluten-free foods was a major barrier to complying with a gluten-free diet, while 83% of the individuals surveyed indicated that finding high-quality gluten-free foods was a major obstacle 62. There have been recent improvements in availability in the marketplace making them easier to obtain. The gluten-free diet is becoming more popular among those 18

28 without celiac disease, being perceived as healthy and tasty 63. A recent survey found that about 30% of adults claim to cut down or completely avoid gluten 64. With more individuals adopting a gluten-free diet, more options will become available in order to accommodate this diet choice. As of 2009, products labeled as gluten free have exploded into an almost $1 billion business, with sales increasing at an exponential rate 63. The increase in demand is driving manufacturers to develop technologies to produce more gluten-free options. With increased availability of products usually comes lower cost, making products easier to purchase for consumers. Additionally, more restaurants are catering to the gluten-free population, offering gluten-free options or special glutenfree menus. Clearer labeling, increased availability, decreased cost and more options at restaurants can lead to a higher quality of life in individuals with CD following a glutenfree diet. Quality of Life Some individuals with CD following a gluten-free diet have reported to have a lower quality of life after their diagnosis. Quality of life is described as an allencompassing perception of health and wellbeing, influenced by and impacting on all aspects of our lives 65. Eating not only meets the physiological need for nutrients, but can be a very communal event. It is interwoven into the fabric of our lives, culture, social, and emotional needs. In the United States, adherence to a gluten-free diet is associated with a negative impact on the quality of life, especially in the social domain. Individuals with CD can face many barriers with adherence to the gluten-free diet, including inadequate food labeling, cost of gluten-free products, using wheat as an additive to many foods, of knowledge of ingredients used in restaurants, and lack of public awareness and 19

29 acceptance of the concept of gluten-intolerance by the public and health care providers 15-16,60,65. For these reasons, lifelong adherence to a gluten-free diet has the potential to negatively affect the economic, social, and physiological domains of quality of life. However, recent advancements in gluten-free labeling, products, and availability has made eating gluten-free easier 6. Starting in 2006, wheat used in products was identified on the ingredient label 66. More recently, the Food and Drug Administration (FDA) has been working to define gluten-free to eliminate uncertainty about how food producers may label their products and to assure consumers who must avoid gluten foods that are labeled gluten-free meet a clear standard established and enforced by FDA 67. Clearer labeling will help those following a gluten-free diet with adherence. Conclusion In summary, CD and the gluten-free diet have become more prevalent in society within recent years. A gluten-free diet is the only acceptable treatment for CD but can be both physiologically and psychologically difficult. Because malabsorption occurs in individuals with CD, weight status and weight change is of particular concern. Barriers to following a strict gluten-free diet can be multifaceted. Although CD is more prevalent now, the cost of the gluten-free diet continues to be expensive and can pose challenges for food insecure individuals or those on food assistance programs. Additionally, the lack of knowledge towards gluten-free foods in regards to nutrition, shopping, and food preparation may also hinder compliance. Therefore, more research is needed to better determine the weight status, gluten-free food availability, and consumer behaviors of individuals with CD, so efforts can be made to improve the overall quality of life for these individuals. 20

30 Chapter 3: Methodology Research Overview The purpose of this study is to describe the weight status, weight change, food security, and consumer behaviors of individuals with CD. There is a need for more research to describe the profile of participants with CD, identify their weight status and food procurement and preparation habits. Additionally, recent research points to the need for more evaluation of socioeconomic factors as related to celiac disease. Research Questions: 1. What is the weight status of individuals with CD? 2. What is the history of weight change in individuals with CD? 3. What is the food security status and food assistance program participation in individuals with CD? 4. What types of consumer behaviors do individuals with celiac disease have? NHANES Overview The National Health and Nutrition Examination Survey (NHANES) is a program of studies that are used to assess the health and nutritional status of adults and children in the United States. The series of surveys combine both interviews and physical examinations and is responsible for producing vital and health statistics for the Nation. It is a major program of the National Center for Health Statistics (NCHS) and is part of the 21

31 Centers for Disease Control and Prevention (CDC). The survey examines a representative sample of about 5,000 persons each year, located in counties across the country. The NHANES interview consists of demographic, socioeconomic, dietary, and health-related questions while the examination part consists of laboratory tests and medical, dental, and physical measurements. Data from NHANES are used to determine the prevalence of major diseases and their risk factors, to create national standards for certain anthropometrics, and to develop health policies, health programs, and series. Subjects Subjects analyzed included those positive for CD, 6 years and older, from , , , and Subjects were excluded if they were pregnant at the time of assessment. Because growth and nutritional data are assessed differently for children and adults, the analyses will be stratified by 18 years and >18 years of age. Data Collection and Preparation Demographics Demographic data were collected in-person with an interviewer using the computer-assisted personal interview (CAPI) software program. Persons 16 years of age and older and emancipated minors were interviewed directly, while a proxy provided information for persons less than 16 years of age and for those who could not answer the questions themselves. Demographics measured include age, gender, race, citizenship, marital status, pregnancy status, education, income, and poverty income ratio. Celiac testing The prevalence of CD was determined using the two step serological testing using the tissue transglutaminase assay (IgA-tTG) and the endomyseal antibody assay (IgA 22

32 EMA). The first level test is the tissue transglutaminase IgA ELISA test. For patients who test positive in this test, the endomysial antibody by immunofluorescence is then carried out for confirmation. A double-positive test is operationally defined as celiac disease. Anthropometrics Anthropometrics were collected during the Mobile Examination Center (MEC) visit. Weight was collected from each participant using a digital floor scale and measured to the nearest 0.1 kilogram. Standing height was measured using a wall-mounted stadiometer and made to the nearest millimeter. The mid-arm circumference was measured with a tape measure and triceps and subscapular skinfolds were measured with a skinfold caliper. Both measurements were made to the nearest 0.1 millimeter. Waist circumference was measured using a tape measure at the uppermost lateral border of the hip crest. Body mass index (BMI) was calculated using the participants height and weight. Waist circumference (WC) was calculated using the WC values measured for each individual. BMI values were recoded to categories per the CDC. We recoded WC based on the values of 88 centimeters for females and 102 centimeters for males. Weight history Weight history questions were asked to participants in the home interview, using the CAPI system. Topics related to body weight were recorded, including self-reported weight over the lifetime, self-perception of weight, attempted weight loss during the past 12 months, and methods used to try to lose weight and to keep from gaining weight. Food security and food assistance Food security data were collected through a personal interview based on four topics: Household food security, individual food security, Food Stamp program benefits, 23

33 and Women, Infants, and Children (WIC) program benefits. Household food security was measured using the US Food Security Module (US FSSM) questions, which refer to all household members. Individual food security items were given to all survey participants in the households that affirmed any FSSM item during the household interview. Questions were administered after the 24 hour recall in the MEC. Food Stamp program benefits questions were collected at the household level. WIC data was not analyzed as it does not pertain to the study. Dietary Behavior and Nutrition Questionnaire (DBQ). Three categorical household-level variables with four response levels were created to characterize the overall food security status for the entire household, the adults in the household, and the children in the household. Household full food security indicated no affirmative responses, household marginal food security indicated 1-2 affirmative responses, household low food security indicated 3-5 affirmative responses without children under 18 years of age; 3-7 affirmative responses for households with children, and household very low food security indicated 6-10 affirmative responses without children under 18 years old; 8-18 affirmative responses for households with children. Households with children that provided no valid response to any of the questions about children s food security were classified using the specifications for households with no child. Consumer Knowledge and Behavior Consumer knowledge and behavior questions were collected through both a household interview and supplementary telephone interview. Information on people s 24

34 knowledge, attitudes, and beliefs towards nutrition and food choices was collected for each participant. Dietary related consumer behavior included information about the family member s use of a special diet, availability of certain types of foods in the family, food expenditures, time spent on food shopping and cooking dinner, and meals eaten together as a family was collected for each participant. Statistical Analysis Descriptive analyses was done of dependent variables for individuals presenting with CD. Analyses were stratified for a single positive serological test and doublepositive. Proportions of responses for weight status, race, age, food security and consumer behavior were determined by Americans with CD. Due to the small sample size and the errors in estimating a nationally-representative sample from a small cohort, the analyses were conducted without the population weight commonly used in NHANES analyses. 25

35 Chapter 4: Results and Discussion The results of this study help to provide a new clinical profile of those testing positive for celiac disease. Although it is known that a diagnosis of CD requires more than just positive serological markers, we operationally define celiac group in this study as the double positive tested group. Our sample of individuals comes from people who participated in NHANES who had measured serological indicators for CD. In regards to demographics, the celiac group was comprised of 57% male and 43% female (Table 1). The participants testing positive for only the tissue transglutaminase test (TTG+) had a similar proportion to the celiac group that were male. Those with celiac disease were mostly non-hispanic white (90%) with a small proportion (5%) as Mexican American. More than half (63%) were married and had incomes >185% of the federal poverty rate (58%), while 17% were <100% of the federal poverty rate. Over three-quarters (79%) of the celiac group were fully food secure; however, 8% had participated in food stamps within the last 12 months (Table 2). 26

36 Celiac Disease (double +) TTG+ Total Variable Category N % N % N % Gender Male 24 57% 26 54% 50 56% Female 18 43% 22 46% 40 44% Race/ Mexican American 2 5% 12 25% 14 16% Ethnicity Other Hispanic 0 0% 1 2% 1 1% Non-Hispanic White 38 90% 23 48% 61 68% Non-Hispanic Black 1 2% 11 23% 12 13% Other or Multiracial 1 2% 1 2% 2 2% Marital Married 22 63% 26 60% 48 62% Status Widowed 5 14% 6 14% 11 14% Divorced 2 6% 6 14% 8 10% Separated 0 0% 1 2% 1 1% Never married 5 14% 4 9% 9 12% Living with partner 1 3% 0 0% 1 1% Income <100% poverty rate 2 17% 2 7% 4 10% Categories % poverty 3 25% 9 33% 12 31% rate >185% poverty rate 7 58% 16 59% 23 59% Table 1: Demographic Characteristics of Serologically Positive Participants 27

37 Celiac (double +) TTG+ Total Variable Category n % n % n % Body Mass Index Underweight 1 3% 3 7% 4 5% categories Norma Weight % 14 33% % Overweight 9 26 % 18 42% % Obese % 8 19% % Has central obesity a % 25 63% % How do you consider your Overweight % 17 39% % weight Underweight 1 3% 4 9% 5 6% About the right weight % 23 52% % Like to weigh more, less or same More 4 11 % 5 11% 9 11 % Less % 20 45% % Same % 19 43% % Tried to lose weight in past year 7 21 % 5 13% % Household food security category Fully Food Secure % 25 93% % Marginally Food Secure 1 7% 2 7% 3 7% Low Food Secure % 2 5% % Very Low Food Secure 0 0% 0 0% 0 0% Participating in food stamps in past 12 mos 2 29 % 1 8% 3 15 % Self-perceived vegetarian 1 4% 0 0% 1 2% Has food allergies 3 11 % 2 10% 5 10 % Allergic to wheat 2 7% 1 5% 3 6% a Central obesity classified as a waist circumference >88 cm for females, 102 cm for males Table 2: Weight, Behavioral, and Socioeconomic Characteristics of Serologically Positive Participants 28

38 The weight profile and views on weight status provides new insight for the weight status of those with celiac disease. Almost 2/3 of the group was overweight or obese according to their body mass index (BMI); however, the average BMI of this group was 25.9 kg/m 2, which is considered overweight. About half of this group presented with central obesity. With regard to perceive weight status, 2/3 of the group consider themselves to be about the right weight; however, the majority would like to weigh less or stay the same, with 21% stated that they had tried to lose weight within the past year. Those participants who tested positive for only the tissue transglutaminase test (TTG+) had varied BMI values, but more than half had central obesity (63%) and consider themselves to weight the right weight (52%). We also examined trends in self-reported weight history. The celiac group stated that they would like to weigh less or the same than their current self-reported weight, and currently weigh less than their self-reported greatest weight (Table 3). According to the self-reported weights, on average, they would like to weigh less than one year ago and ten years ago. However, their average weight change from one year ago was only about a loss 1.5 pounds, while their average weight change from ten years ago was approximately one half-pound of weight gain. The individuals in the group who tested positive for only the TTG+ test stated that on average, they would like to weigh less than their current selfreported weight, currently weighed more than self-reported weight one year ago, and matched their self-reported weight from ten years prior. When exploring dietary constraints, we noted that only 11% of the individuals in the celiac group had food allergies, and 7% were allergic to wheat (Table 2). Since this is self-reported data, whether this is a known wheat allergy, an intolerance to wheat, or a 29

39 Celiac Disease (n=42) TTG+ (n=48) Total (n=90) Mean SD Mean SD Mean SD Body Mass Index (kg/m 2 ) Waist circumference (% of threshold central obesity value) Current self-reported weight (lbs) How much would like to weigh (lbs) Self-reported weight - 1 yr ago (lbs) Self-reported weight-10 yrs ago (lbs) Self-reported weight-age 25 (lbs) Self-reported greatest weight (lbs) Age when heaviest weight (yrs) Weight change from 1-yr ago (lbs) Annual weight change from 10-yr ago (lbs) Table 3. Weight Characteristics of Serologically Positive Participants gluten intolerance is unknown. Few individuals reported themselves to be a vegetarian (<5%). The consumer behavior data provided detail into the food behavior and food consumerism for this population. For the celiac group, less than half were the main meal planner, participate in meal preparation, and main food shopper (Table 2). They reported eating an average of four meals that were not home prepared and three meals from a fast food or pizza place within the past week. At home, they stated to eat, on average, 1 meal comprised of ready to eat foods and 6 frozen meals or frozen pizza within the past 30 days (Table 4). 30