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Celiac disease and food allergies have been increasing in prevalence over the past few decades,1-3 causing reduced quality of life in patients with these disorders, and are becoming serious public health concerns nationwide. Dental healthcare professionals play a significant role in the management of conditions that may result in digestive disturbances, such as food allergies, food intolerance, and celiac disease. In addition, dental healthcare professionals are ideally positioned to identify celiac disease and pollen-food allergy syndrome, as these conditions may present with a number of oral manifestations.4-6 Treatment of these disorders may itself potentially further impact the patient's oral health in certain instances, while the patient's individualized dental treatment plan must also take into consideration the special dietary restrictions these patients must observe. To appropriately manage the oral health of these patients, it is essential that dental clinicians have up-to-date clinical information on the dietary needs and restrictions that are necessary, particularly with regard to avoiding the use of dental products that may contain contraindicated ingredients.
Once believed to be a rare condition, celiac disease (CD) has increased in prevalence significantly over the past three decades.1 CD is a lifelong autoimmune disease triggered by gluten ingestion in genetically susceptible patients. While the etiology of CD appears to involve genetic predisposition, immunologic factors, diet, and environmental triggers, CD can develop at any age and occurs most commonly in females. Dentists are often the first healthcare professionals to recognize potential CD in children, as the first recognizable signs in pediatric patients often present in the oral cavity.4 CD has a wide range of signs and symptoms that mimic other diseases, making it extremely difficult to accurately diagnose. In fact, initial results of a current ongoing mass-screening program (ASK study) reveal a high prevalence of undiagnosed CD in children in the United States.7This has significant implications, as undiagnosed CD can predispose the affected individual to other autoimmune diseases, especially type I diabetes.8
The pathogenesis of CD involves the gluten proteins, gliadin and glutenin, as the trigger for an immunologic response. While the intestinal epithelium in a healthy individual acts as a barrier to the passage of these gluten proteins, the patient with CD has compromised epithelial function. In patients with CD, large peptide fragments are thus able to penetrate through the epithelium into the lamina propria, causing a T cell immune response. This results in inflammation of the small intestine, leading to flattening of the intestinal villi of the mucosa and malabsorption of nutrients.9,10 Absorption of macronutrients and micronutrients is essential for the proper development of healthy dentition in children4 and for maintenance of healthy dentition in adults.
CD has a wide variety ofsystemic and oral signs and symptoms, which can vary from person to person and can occur at any age. While the first recognizable symptom in children is frequently an oral manifestation,4 children also typically present with gastrointestinal symptoms including vomiting, diarrhea, bloating, flatulence, and/or abdominal pain.1 The most common oral symptoms of CD seen in children include recurrent aphthous ulcers, reduction of salivary flow, and dental enamel defects.5 Adults may experience gastrointestinal symptoms, anemia, osteoporosis, infertility, neurological manifestations and/or dermatitis herpetiformis, the skin form of CD.11 If the patient has been suffering with CDfor many years without proper diagnosis, they may have vitamin deficiencies, resulting in atrophic glossitis.10,12A cutaneous form of CD, dermatitis herpetiformis, presents as a chronic skin rash on the elbows, knees, or buttocks.4If CD is suspected, the dentist should refer the patient to a gastroenterologist for evaluation and diagnosis. Because there is no one single medical diagnostic test to support the diagnosis of CD, the best way to determine the diagnosis is through both a positive blood test and positive biopsy results.13
Although research is underway to develop a pharmacologic therapy to treat CD,14 currently there is no cure for this disorder. For symptom resolution and regeneration of small intestine villi and recovery, to date the only treatment is a strict gluten-free diet.1 Therefore, patients with CD can benefit from a referral to a registered dietitian to help them completely avoid all forms of gluten. The dietitian can be instrumental in helping the patient achieve a healthier lifestyle, by evaluating the patient's current dietary intake to confirm that it is nutritionally adequate, assisting the patient in choosing nutritious, gluten-free grains, and helping him or her avoid cross-contact with foods containing gluten.4A strict gluten-free diet has been shown to have a positive impact on the oral health of children with CD in terms of both reduced rate of caries15 and lower plaque index.16A recent observational study by Nota et al evaluating 237 adults with CD found a correlation between strict adherence to a gluten-free diet prescription and a decrease in both gingival bleeding and nocturnal snoring.17 The authors state that "following a gluten-free diet appears crucial to managing oral diseases associated to celiac pathology." In addition, they suggest that the general dentist "should implement a specific clinical protocol for celiac patients [that includes] frequent follow-ups with monitoring of ‘general' health in addition to oral health."17 The authors also concluded that following a gluten-free diet could be important in controlling gingival bleeding levels and managing oral symptoms associated with CD.
Although there are labeling laws that apply to gluten-free labeling on food products, they do not apply to dental products or medications. In clinical practice, it is has been the authors' experience that patients with CD often worry about potential gluten in oral care products. Most manufacturers of dental products will disclose which products are gluten-free on their website as well as on the product label. While there have been very few studies examining the gluten content in oral care products, recent research by Verma et al revealed that most toothpaste, dental tablets, and mouthwash have very low gluten levels.18 Three of the toothpastes tested in this study did have more than 20 ppm of gluten (which is considered higher than the tolerable limit), but the amount of gluten digested during teeth brushing would still be negligible with these products. These authors concluded that the amount of gluten that may be present in oral care products on the market "is not an issue" for patient with CD."18 However, in our opinion, there is the potential for an additive effect with the use of oral care products and medications that contain gluten, and the level of gluten thus consumed may become enough to elicit symptoms. As part of the dental treatment plan for patients with CD, dental clinicians should therefore consider potential sources of gluten (eg, wheat starch) that may be present in over-the-counter and prescription medications and recommend that these patients avoid those medications.4The clinician can obtain information about the gluten content of medications on the internet through various websites17 or by checking with the pharmacist.
Because maintaining a gluten-free lifestyle requires constant vigilance, patients with CD will benefit tremendously from multidisciplinary collaboration among their gastroenterologist, primary care physician, registered dietitian, and dental clinician.
Although the terms food intolerance and food allergy are often used interchangeably, a food intolerance is a non-immune-mediated digestive disturbance. The most common food intolerance is lactose intolerance (LI), which is the inability to completely break down the milk sugar, lactose, into two simple sugars, glucose and galactose. This results in gastrointestinal complaints after the individual with LI has consumed dairy foods. While there are differing levels of intolerance and symptoms, which vary from patient to patient, most patients with LI can tolerate small amounts of dairy and lactose without experiencing symptoms.19 Very little research is available on the oral health of children with LI. A cross-sectional study by Moimaz et al examining caries risk in Brazilian children with LI found that caries prevalence and severity was higher in these children than in those without LI.20 The researchers recommended early intervention to prevent caries in this high-risk group.20Because it is well-known that dental caries is a diet-related disease, with fermentable carbohydrates necessary to promote its development,21 the dental clinician should keep in mind that a referral to a registered dietitian may be appropriate for a pediatric patient with LI.
Another common food intolerance is intolerance to FODMAPs (Fermentable Oligo-, Di-, Mono-saccharides, And Polyols). These small, nondigestible carbohydrates are poorly absorbed in the small bowel, causing gastrointestinal symptoms in most patients with irritable bowel syndrome. The severity of symptoms varies from patient to patient. Many of these patients experience resolution of their symptoms when they limit or avoid foods that contain FODMAPs. FODMAPs are found in a wide variety of foods and sweeteners, including sugar alcohols.22Clinicians should be mindful that many patients who need to follow a low FODMAP diet must either limit or completely avoid sugar alcohols.
Research suggests that frequent use of xylitol is associated with significant reduction in the incidence of dental caries.23In addition, products containing xylitol, such as sugar-free gum, lozenges, and oral melts, are often recommended to patients suffering with radiation-induced xerostomia.24Dental clinicians must be aware that xylitol is a sugar alcohol and may cause gastrointestinal distress in a patient who is on a low FODMAP diet. Therefore, a xylitol-based caries program or xylitol-containing products to treat xerostomia would not be recommended for such patients.
A food allergy is defined as an adverse immunologic response to a food protein.25The prevalence of food allergies has been increasing over the past several decades, severely impairing the quality of life of affected individuals and their families. According to recent studies, 5.6 million children2 in the United States and more than 26 million US adults3 have a food allergy.
The pathogenesis of a food allergy involves a sensitization phase, which progresses to a true clinical food allergy. In the case of a true food allergy, an IgE-mediated response occurs to a food protein every time the individual eats the food to which they are allergic. Symptoms such as urticaria, angioedema, coughing, wheezing, abdominal pain, vomiting, and in severe cases, anaphylaxis, typically occur within minutes after eating the food. While a second-generation antihistamine is recommended for a mild allergic reaction, epinephrine is the first-line treatment for anaphylaxis.26Anaphylaxis is a serious allergic reaction that can be fatal if not treated immediately.
Avoidance of the allergen is the only currently recommended treatment for patients with a food allergy. However, even a trace amount of an allergen may be enough to elicit a severe reaction and anaphylaxis, and it is very difficult to avoid all sources of allergens. Although there are labeling laws that apply to potential allergens in food products, they do not apply to dental products or medications. For this reason, dental patients who have allergies are often concerned about potential allergens in oral hygiene products. All in-office dental materials and products, including prophylaxis paste, must be free of allergens and allergen cross-contamination. Clinicians must also be aware that allergens can often be hidden in "natural flavorings." The most commonly occurring food allergen used in the dental office is themilk protein, casein. Therefore, the compound casein phosphopeptide-amorphous calcium phosphate (CPP-ACP), which has been shown to have a synergistic effect on enamel remineralization when combined with fluoride,27 should never be used in a dental patient with a known milk allergy. Dental professionals should therefore always check for potential allergens in medications before providing them to their patients with food allergies. It is often necessary to contact the manufacturer directly in order to determine which dental products and medications are safe for these patients.
A medical consult to a board-certified allergist may be appropriate to confirm the diagnosis of a food allergy, since many patients confuse a true food allergy with a food intolerance.2,3 Because an allergen-free lifestyle requires constant vigilance, communication and collaboration with other healthcare providers are imperative for patient-centered care.
Moimaz et al found that children with milk allergy had a higher prevalence and severity of caries.20 When dairy products are being eliminated from the diet of child with a milk allergy, a decreased intake of calcium often results, and because calcium is needed for a healthy dentition, the oral health of the child may be at risk. Therefore, children whose diet has been modified to address their milk allergy are considered to be at high risk for caries and need appropriate interventions for caries prevention. This often includes a referral to the registered dietitian for nutritional counseling.
POLLEN-FOOD ALLERGY SYNDROME
Pollen-food allergy syndrome (PFAS), formerly known as oral allergy syndrome, requires prior sensitization to a cross-reacting inhalant allergen. Aeroallergens include birch, ragweed, and grasses.28The proteins in the pollens are similar to the proteins in certain raw fruits and vegetables, which causes the patient's immune system to mistake the food for the pollen, resulting in a reaction. Symptoms are usually mild, and the patient is instructed to avoid the raw form of the food. PFAS is a common condition, affecting a significant portion of the population, with a prevalence of approximately 4.7% to 20% in children and 13% to 53.8% in adults.29
The dental clinician may be the first healthcare professional to recognize this syndrome, as symptoms are typically isolated to the oropharyngeal region.6,29 Symptoms include pruritus of the oral mucosa, including the lips, mouth, gingiva, tongue, and throat.6 Patients with PFAS experience symptoms immediately after eating certain raw fruits, vegetables, spices, or nuts. The symptoms may continue for a few minutes after eating the food. Patients allergic to birch may be cross-reactive to multiple fruits, vegetables, and nuts, including apples, pear, sweet cherry, peach, plum, apricot, almond, and hazelnuts.30,31 Ragweed has been associated with banana, melons, kiwi, and peaches.6Grasses have been associated with tomato, peach, and apple.6
Because of the lability of the food proteins causing the reaction, often these patients are able to tolerate the cooked form of the food, as these proteins become denatured. Therefore, for patients with PFAS, the offending foods can be baked or microwaved to change the configuration of the protein and thus avoid causing symptoms in susceptible individuals. Avoidance of the raw form of the fruit or vegetable allergen is the only current treatment for PFAS. However, allergen immunotherapy (ie, allergy shots) may lessen the severity of symptoms.
The dental clinician should refer the patient to a registered dietitian for evaluation and dietary advice. Although it is very uncommon for PFAS to lead to severe symptoms, if the patient experiences worsening symptoms, has symptoms even after the offending food is cooked first, has symptoms to nuts, or has a known IgE-mediated reaction to any food, the patient must be referred to a board-certified allergist for evaluation.32
As the prevalence of celiac disease and food allergies continues to rise, one of the important challenges faced by dental clinicians today is the ability to remain up to date on the clinical guidance for the management of patients with these conditions, as well as those with food intolerances. Patient health and safety are paramount concerns when dental healthcare professionals are treating these patients. Often the first healthcare professional to identify celiac disease and pollen-food allergy syndrome, dental clinicians have a unique responsibility not only in recognizing the signs and symptoms of these disorders, but in helping patients avoid the disease triggers, both in the products used in the dental office and those used at home. Likewise, dental healthcare professionals must be aware of the dental care products that contain food allergens or ingredients that need to be avoided by patients with a food intolerance, and they should understand the risk of caries and other oral health risks experienced by patients with food allergies and food intolerance. Finally, dental clinicians must be mindful about when to refer patients to specialists, including dietitians, and about the vital importance of multidisciplinary collaboration with other healthcare professionals when caring for these patients.
About the Authors
Ellen Karlin, MMSc, RDN, LDN, FADA
Private Practice, Scottsdale, Arizona
Sara Karlin, DDS
Board-certified Pediatric Dentist
Private Practice, Phoenix, Arizona
Clinical Adjunct Assistant Professor
Arizona School of Dentistry and Oral Health
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