As COVID-19 restrictions ease across Canada, many individuals will be heading back to the dentist for their regular cleanings and delayed appointments. One of the atypical signs of celiac disease is found in the mouth. We asked Melissa E. Ing, D.M.D. to provide an overview of the impacts of celiac disease and gluten disorders on your oral and dental health.
THIS ISSUE HAS BEEN GENEROUSLY SPONSORED BY QUEEN STREET BAKERY
The Academy of General Dentistry states that more than 90% of systemic diseases have some sort of oral connection. There is a growing link between oral and general health which put dentists in the frontlines to help detect systemic disease. This is especially true with celiac disease.

In the United States, 27 million people visited the dentist more often than the physician. These statistics vary here in Canada, most likely due to the differences in health care coverage.

According to Costa Papadopoulos, Canadian Dental Association's Health Policy Manager, Statistics Canada data indicate that in 2010 more than 13% of Canadians consulted a dentist and not a medical doctor.

The health professions need to work “inter-professionally”. That means: medical, dental, and nutritional teams can work together to diagnose more rapidly and to better control celiac disease for those that suffer.

Currently, there is an average of 6-10 years delay for a celiac patient to get diagnosed. If the dental team can be made aware of the breadth of celiac disease and its related oral symptoms, a timely medical referral and subsequent diagnosis can occur.

It is equally important for celiac disease patients to recognize, understand, and control associated oral manifestations.

SOMETIMES DENTAL CLUES ARE THE ONLY INDICATION OF CELIAC DISEASE

While some celiac disease patients can present with a multitude of bodily symptoms, including: gastrointestinal symptoms, anemia, joint pain, or osteoporosis, while others can have “asymptomatic celiac disease”. That means the ONLY celiac presentations might be some dental clues that appear in the oral cavity.

Children and adults with celiac disease can have similar oral manifestations. Some of the most common oral manifestations include “dental enamel defects” and “recurrent aphthous ulcers”.

Dental enamel is the hardest substance in the body. It is the visible white outer surface of the teeth. Children with celiac disease often present with “dental enamel defects”. In fact, there are studies, such as that by El Hodhod et al., demonstrating that children with celiac disease have more dental enamel defects than those in the general population. According to El Hodhod as well as other researchers, dental enamel defects may possibly be the only manifestation of pediatric celiac disease.
Dental enamel defects may possibly be the only manifestation of pediatric celiac disease – El Hodhod et al.
Dental enamel defects are permanent abnormalities which form as the enamel develops. Enamel is not a living tissue so it cannot naturally regenerate or repair itself. Dental enamel defects can sometimes have the appearance of thinner, more translucent-than-normal enamel layer so that the underlying yellowish dentinal layer shows through. In addition, children can develop what is called “mottled enamel” which means that enamel will not be naturally shiny, white and uniform. Some patients may also have “pits” or horizontal “bands” within the enamel of their teeth. The enamel can also be discoloured, with white, yellow or brown spots within the enamel.

Dental enamel defects always appear “bilaterally” or “symmetrically”, which means that they are found on BOTH sides of the mouth at the SAME time. Some teeth are more susceptible to enamel defects due to the chronological development of the permanent dentition. Incisors, then first molars calcify prior to the other teeth in the mouth. Therefore, permanent incisor teeth followed by first molars are most often seen with dental enamel defects in CD patients.

Dental enamel defects are not as prevalent in adult patients with celiac disorder. This is possibly because the defects are cosmetically corrected by adulthood with bonding or veneers.

Research studies by De Carvalho et al. demonstrated that enamel of pediatric CD patients have less of a calcium to phosphorus ratio. There are theories that malabsorption of calcium and immunological factors associated with celiac disease are responsible for enamel abnormalities.
The jury is out as to whether children with celiac disease are more prone to dental decay. Several studies, including that of DeCarvalho et al., demonstrated that children diagnosed with celiac disease, and controlled with gluten-free diets, were found to be possibly protective against having tooth decay. DeCarvalho hypothesized that gluten, which is made up of several proteins, is found in “cariogenic foods” (foods that promote decay) such as oatmeal, breads, crackers, and regular flour.
Yet there are other studies, including that of Cantekin et al., demonstrating children with celiac disease tend to have more decayed, missing, or teeth with fillings, than children who do not have celiac disease.

Children with celiac disease have delayed skeletal development and they can also have delayed eruption of teeth as well. Multiple documentations such as those by Paul et al. demonstrate that celiac children have a much higher potential for delayed tooth eruption compared to children without celiac disease.

Children and adults with celiac disease often have “recurrent aphthous ulcers” inside the mouth. These appear as 2 to 8 mm round or ovoid yellowish lesions with defined borders. They are usually located inside the lips, inside of the cheeks, or on the undersurface of the tongue. The ulcers are painful and can last up to two weeks in time. The ulcers will come back at different periods of a patient’s lifetime so that is why they are termed “recurrent”. The consumption of spicy or salty foods and stressful situations tend to exacerbate the lesions. Warm saltwater rinses and avoiding spicy foods may bring some relief when these ulcers appear.
DeCarvalho also documented that children with celiac can possibly also have reduced salivary flow.

Celiac disease patients tend to have dry mouth which is called “xerostomia”. Xerostomia can feel like a burning, uncomfortable sensation. There are conflicting reports as to whether dry mouth conditions promote more cavities in celiac patients since there is less saliva to wash away debris. Xerostomia can be treated by frequently hydrating with water or by trying some of the over the counter commercial mouth rinses specifically formulated to treat dry mouth. Many of these do not contain gluten and there is one on the market that is free of sodium lauryl sulfate, which will be more soothing to the mouth.

Patients with celiac disease can possibly have irritated tongue conditions. A healthy patient’s tongue is usually a light pink colour on its surface, which is called the ‘mucosa”. The mucosa is covered with tiny little bumps called “papillae”. Papillae are responsible for taste and speech. The papillae provide a robust protective surface during chewing and swallowing.

Sometimes, the tongue can have an inflammatory response if there is a related malnutrition, a local infection, a drug reaction, or perhaps a systemic condition such as celiac disease. These tongue conditions can be exacerbated due to anemia or vitamin B complex deficiencies.

With inflammatory conditions the mucosa losses its normal, light pink colour because the papillae become atrophic (thin out). Celiac disease can be associated with two types of tongue conditions: “atrophic glossitis” or “geographic tongue”.
Once celiac patients are diagnosed and are following a strict gluten-free diet, inflammatory tongue conditions can heal.
With “atrophic glossitis” the mucosa loses its light pink colour and becomes glossy, smooth and bright red because the papillae disappear. Atrophic glossitis can be associated with dry mouth and loss of taste. Patients complain of burning sensation. Discomfort can be alleviated by lifestyle changes, including the avoidance of spicy or too hot food, quitting smoking, and limiting alcohol. Celiac patients may suffer from nutrient deficiency so vitamin B12, an iron rich diet, or iron supplements may help.

When patients have “geographic tongue” only portions of the mucosal papillae are denuded so that there is an irregular appearance on the surface. These irregular patterns can change daily and actually appear to look like a map, hence the moniker “geographic”.

Once celiac patients are diagnosed and are following a strict gluten-free diet, inflammatory tongue conditions can heal. If villous atrophy of the small intestine resolves there should be less iron and vitamin depletion so the oral mucosal papillae will grow back.

Adults and children with celiac disease can also have “angular cheilitis”, a condition that causes swollen patches at the CORNER of the mouth where the upper and lower lips meet.
This can be accompanied by bleeding, cracking, and crusting. The lesions can be slow to heal because the affected surfaces are mobile during mouth movements, such as opening and closing; and subject to repeated wetting and drying from saliva exposure. People that have immune disorders, dry mouth, ill-fitting dentures, or lack posterior teeth support are more prone to angular cheilitis. Iron and vitamin deficiencies can contribute to angular cheilitis. Therefore, the dental team may recommend vitamin B complex supplements and possibly an antibiotic ointment for celiac patients suffering from angular cheilitis.

While not as common, “ oral lichen planus”, can be a symptom of celiac disease patients. Oral lichen planus usually presents as lacy white patches or bumps on the inside of the cheeks, roof of the mouth, on the tongue or inside of the lips. Patients may complain of a scratchy dry feeling. Another type of oral lichen planus presents as red, swollen open sores which can often be found at the gum area. This type of oral lichen planus is considered “erosive” and patients will complain of a burning, painful sensation. Cigic et al.’s study demonstrated that oral lichen planus is more prevalent in celiac patients compared to the general population.

Reports of oral cancer are not as common as some other oral manifestations found in adult celiac disease patients.  Squamous cell carcinoma can be found in the mouth extending back to the area leading to the esophagus. These lesions can appear as irregular, rough, or eroded red or white patches that may be ulcerated. They can be located anywhere in the mouth. The areas under the tongue and at the floor of the mouth are especially susceptible. The lesions can be painful, making it difficult for individuals to consume food or drink. If these suspicious-looking lesions persist and do not go away in 14 days then the dentist may order a biopsy to rule out oral cancer.
CCA HAS A FACT SHEET DEVELOPED BY OUR PROFESSIONAL ADVISORY COUNCIL ON CELIAC DISEASE AND THE ORAL MANIFESTATIONS.
Celiac patients should not have to worry about being inadvertently ‘glutened’ from over the counter oral health products, cosmetics, lipsticks, lotions or creams. Furthermore, patients should be able to look forward to dental office visits without worrying about possible adverse gluten reactions mounting from materials the dental team introduces into the oral cavity.

Unlike commercially processed food products there currently is NO accepted gluten-free threshold measurement labeling for health, beauty, or oral care products. Health Canada’s Marketing Authorization permits manufacturers to use the (GF) symbol on commercially-packaged FOOD products that contain less than 20 parts per million of gluten.

TESTING DENTAL PRODUCTS FOR GLUTEN:
DENTAL MATERIALS, SOAPS, LOTIONS AND ORAL HEALTH PRODUCTS

In two studies we tested 30 dental materials that would be commonly used in restorative filling procedures. We also tested the materials that would be utilized during a dental cleaning as well as the materials that would be used during a typical endodontic (root canal) appointment. We also analyzed the bactericidal soap and hand lotion that is used in the Tufts University dental clinics. The hands might possibly touch a celiac patient’s mouth during dental treatment so it is important that the soap and lotion used it gluten free.

We found that all the materials tested contained less than 5 PPM, which is well below the acceptable 20 PPM range. Therefore, our studies determined that the materials currently being used for the filling procedures, the prophylaxis procedures, and root canal procedures at Tufts are not putting celiac disease patients at risk of gluten exposure.

Since the list of dental materials and over the counter oral and health and beauty products is vast and variable, more R5 ELISA research testing would be prudent to keep CD and gluten sensitive consumers safe
TELL THE DENTAL TEAM OF CELIAC DISEASE OR GLUTEN INTOLERANCE

A newly diagnosed celiac patient should inform the dental team of their changed medical history status prior to their next oral care visit. Giving a heads up is a win-win so the dental team can prepare, and the patient will get the most out of their future dental visits. Here are some tips:

  • The patient should advise the dental team in advance of the recent diagnosis of celiac disease. This gives the dental providers the opportunity to familiarize with the parameters of celiac disease. 

  • The patient should ask the dental team to research the routinely used dental materials in cleanings and filling procedures to see if they contain gluten. The dental office will need to contact each dental manufacturer to obtain this information.

  • Manufacturers of dental materials may say that their materials are gluten free but to be accurate materials need to be individually tested via ELISA gluten analysis, as discussed in Dr. Ing’s research studies.

  • Medical history of the patient needs to be updated the day of dental visit at the office. 

  • Since there is a hereditary component to CD the dentist should advise the patient that their family members should be on the lookout for celiac symptoms and may need to seek primary care physician consultation.

  • The dental team should perform a thorough extraoral and intraoral exam, including a check for oral manifestations of celiac disease as discussed in this article.

  • The dental team should have recommendations ready for celiac disease patients that complain of oral manifestation irritations such as xerostomia (dry mouth), angular cheilitis (cracks/redness at the corners of the lips), and recurrent aphthous ulcers inside of the mouth.

  • For dry mouth the dental team may recommend dry mouth substitute. Check manufacturers for gluten-free remedies.

  • Lip balm is helpful for dry lips. Since angular cheilitis can be caused by loss of nutrients in celiac patients the dental team may recommend vitamin B complex. Sometimes a prescription for an antibiotic cream is also helpful for angular cheilitis. Sometimes angular cheilitis in adults is caused by ill-fitting dentures so the dentist may recommend a new set.

  • For recurring aphthous ulcers the dental team may recommend warm saltwater rinses and suggest that the celiac patient avoid spicy foods.

  • For inflammatory tongue issues the dental team may recommend vitamin B12 and iron and to avoid spicy foods. Again, once the patient is on a strict gluten-free diet some of tongue and angular cheilitis issues may not occur as frequently.

  • The dental team should review and emphasize oral hygiene instructions that include flossing and decay preventative measures. The dental team may perform a “CAMBRA” assessment, which means caries (decay) management by risk assessment. This is a standard to identify the cause of decay through an individual’s decay risk assessment. It encourages management of these risk factors and is used to determine appropriate preventive and minimally invasive caries treatment.

  • The dental team may treatment plan fluoride varnish applications for at-risk-for-decay patients.  In addition, the dental team may suggest that patients supplement their home care with specially formulated high sodium fluoride toothpaste (5000 PPM) or rinses that may be purchased over the counter in Canada.  


IN SUMMARY
Dentists, hygienists, and physicians can work together to speed up the diagnosis for celiac disease patients. By fostering awareness to both patients and the dental team regarding oral and systemic symptoms; and by encouraging more research, we can dynamically increase the quality of life for celiac patients.
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McMASTER COVID-19 SURVEY NEEDS NON-CELIAC PARTICIPANTS

To date, 10,430 celiac patients and 5,491 non-celiac populations over the world responded to the McMaster COVID-19 survey. Of these, 3750 celiac and 1116 non-celiac completed the survey in Canada.
They are asking the gluten-free community if we could help them get more people completing the survey, especially the non-celiac population.

Can you share the link with 2-3 family and/or friends so they can reach the goal soon?

The link to the people WITHOUT celiac survey is as follows: https://is.gd/covidceliac
GF 101: GETTING STARTED ON THE GLUTEN-FREE DIET

When: Jul 17, 2020 06:30 PM Eastern Time
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ACKNOWLEDGMENTS

Dr. Ing wishes to thank Dr. Edmund Peters, Professor, Division of Oral Medicine, Oral Pathology and Radiology, Faculty of Medicine and Dentistry, University of Alberta, Canada, for his assistance in reviewing this manuscript.

Dr. Ing wishes to thank Dr. Michael Goupil, Associate Professor in the Department of Oral and Maxillofacial Surgery and former Associate Dean of Student Affairs, University of Connecticut School of Dental Medicine, Farmington, CT, for his assistance in reviewing this manuscript.

ABOUT THE AUTHOR

Dr. Melissa Ing is a Native Canadian. She obtained her Bachelors of Science, majoring in biology at University of Western Ontario. She graduated with her Doctor of Dental Medicine degree from Tufts University in Boston, Massachusetts.

Dr. Ing has been in dental academia for over 28 years. She was the former Pre-doctoral clinical director at the University of Connecticut School of Dental Medicine (UConn SDM). She is currently an Associate Professor at Tufts. She is involved with designing and delivering courses in cariology (the study of decay), fluoride, dental materials, standardized case notes, and ergonomics. She is involved with different areas of research including: infection control, cariology, ergonomics, public health, educational research, and celiac disease. She is also very involved with STEM education initiatives to encourage young people to consider health science careers.

She has published abstracts, manuscripts, a book chapter on infection control safety, eyewear safety, and ergonomics; and has featured in international interviews, webinars and podcasts, including one on handling COVID-19 dental emergencies.

Dr. Ing is the recipient of the 2015 national Colgate-Palmolive/ADEA (American Dental Education Association) Excellence in Teaching Award and the recipient of two UConn SDM Kaiser-Permanente Excellence in Clinical Teaching Awards. She was nominated for a Tufts University Teaching with Technology Award, for the 2020 Presidential Award for Excellence in Science, Mathematics, Engineering Mentoring, and for the 2020 National Science Board’s Promotion of Science Award.

Dr. Ing is a member of the Commission of Dental Competency Assessments, the Consortium of Operative Dental Educators (Region V Co-Chair and Secretary), Million Women Mentors, American Association of University Women, American Dental Education Association, and the Organization for Safety, Asepsis, and Prevention.
REFERENCES

1.Vujicic, M. et al. Guest editorial-A profession in transition. Journal of the American Dental Association. February 2014.
2.El-Hodhod, Mostafa Abdel-Aziz, et al. Screening for Celiac Disease in Children with Dental Enamel Defects. ISRN Pediatrics. V. 2012.
3.De Carvalho, F.K. et al. Oral aspects in celiac disease children: clinical and dental enamel chemical evaluation. Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology. June 2015. Vol. 119 No.6.
4.Maloney, W. et al. Oral and Dental Manifestations of Celiac Disease. New York State Dental Journal, Hempstead. Vol. 80, Iss. 4. (June/Jul. 2014) 45-8.
5.Cantekin, K. et al. Presence and distribution of dental enamel defects, recurrent aphthous lesions and dental caries in children with celiac disease. Pak J Med Sci 2015; 31 (3):606-609.
6.Pastore, L. et al. Oral Manifestations of Celiac Disease. Journal of Clinical Gastroenterology. Issue: Volume 42 (3), March 2008, pp224-232.
7.Paul, S. P. et al. Coeliac disease in children-an update for general dental practitioners. British Dental Journal. (2016) 220,481-485.
8.Cigic, L. et al. Increased prevalence of celiac disease in patients with oral lichen planus. Clinical Oral Investigations, Apr. 2015 Vol. 19 (3). pp. 627-635.
9.Verma, AK. et al. Contribution of Oral Hygiene and Cosmetics on Contamination of Gluten-free Diet: Do Celiac Customers Need to Worry About? J Pediatr Gastroenterol Nutr 2019; 68 (1): 26-29.
11.Ing, M.E. et al. The Gluten-free Endodontic Dental Visit. Tufts University School of Dental Medicine, Boston, MA. 2019.
12.Ing, M.E. et al. The Gluten-Free Operative Dental Visit and Prophylaxis Dental Procedure at Tufts University School of Dental Medicine. Journal of Dental Education. 2017. Vol. 81, No. 2.
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