Necrotizing ulcerative gingivitis (NUG) is an acute bacterial infection caused by fusiform rods and spirochetes (Borrelia vincentii). When NUG progresses and results in attachment loss, it is referred to as necrotizing ulcerative periodontitis (NUP). Together, NUG and NUP are now classified as “Necrotizing Periodontal Diseases” according to the 1999 classification of periodontal diseases and conditions.1 Necrotizing periodontal diseases are also known as acute necrotizing ulcerative gingivitis (ANUG); ulceromembranous gingivitis; Vincent’s infection and trench mouth.
A combination of the signs and symptoms of NUP are listed in Table 1. Patients with NUG or NUP may have a history of personal stress, poor oral hygiene, cachexia, heavy smoking and poor nutrition with possible vitamin deficiency. A compromised immune system due to systemic conditions such as HIV/AIDS may also be associated. Although the clinical features are unique, the differential diagnosis of NUP includes many other pathological processes (Table 2).
If untreated, irreversible loss of periodontal structures can occur in just a few days. Only very mild forms heal without permanent damage.
Treatment considerations include cleaning teeth by way of irrigation with hydrogen peroxide to remove the pseudomembrane. Antibiotics should be given immediately to avoid significant tissue destruction. Pain control and management of systemic manifestations is also a treatment goal. Oral hygiene instructions should include the prohibition of smoking. An emphasis on nutrition is critical as the painful nature of this condition limits food choices. Despite normal healing, partial loss of the interdental papillae (often referred to as “punched out papillae”) can be expected. A complete periodontal evaluation should be undertaken following the resolution of the acute phase.
J.P., a 53 year old fork lift operator was referred to our clinic in 2005 for management of his periodontal condition (Fig. 1). His medical history was unremarkable aside from smoking approximately 30 cigarettes/day for at least 20 years. He considered himself extremely anxious with respect to dental care due to an admitted needlephobia and did not see the dentist regularly due to this fear. He reported that all his mandibular teeth and some maxillary molars were removed in 1973 due to “pyorrhea.” He reported his occlusion as comfortable, functional and esthetically satisfactory. After clinical and radiographic examination, he was diagnosed with generalized chronic severe periodontitis modified by a smoking habit, local factors, irregular dental care and dental anxiety.
The treatment plan included removing several teeth including the impacted 23. The patient refused the extractions due to no perceived problem. The treatment plan was reduced to smoking cessation counseling, detailed oral hygiene instructions, scaling and root planning with local anaesthesia under intravenous sedation, systemic antibiotics and subsequent re-evaluation. The sanative phase was completed in one appointment. The patient did not return for the re-evaluation and was lost to follow up.
In May 2007, he returned to our clinic with the chief concern of severe pain, loose teeth and bad breath (Figs. 2 & 3). He reported the pain began three days earlier and was escalating in severity. He reported feeling malaised, feverish, unable to eat and in excruciating pain. He was however, still able to smoke.
Clinical examination revealed severe halitosis which was first detected while the patient was still in the waiting room. The papillas were blunted and a grey pseudomembrane was noted interdentally and continued onto the palate over the area of the impacted canine. The remaining erupted teeth were mobile ranging from M2-M3. His plaque score was 100%.
Given the clinical history and presentation a diagnosis of NUP was made. A two stage treatment plan was recommended.
1. Removal of 21, 22, 23, 24 and debridement of the tissues followed by adequate healing to allow impressions for an immediate full upper denture.
2. Subsequent removal of the remaining teeth and delivery of the denture.
Given the patient’s dental anxiety, the first surgery was scheduled under conscious sedation 72 hours from the time of his presentation with NUP. In the meantime he was prescribed an antibiotic and pain control medication and was counseled on his nutritional strategy during his recovery.
He returned for surgery missing 21 and 22 which had fallen out over the weekend (Figs. 4 & 5). Teeth 23 and 24 were removed leaving a sizeable defect that could not be closed by primary intention. The patient returned five days post-surgery and areas of exposed bone were reduced with a Piezo ultrasonic handpiece without the use of local anaesthetic (Figs. 6-9). The extraction site at 23 was collecting debris and this was dressed with Alvogyl (Septodont). The patient returned two weeks post-surgery reporting no problems. The site was healing well, albeit with severe loss of his ridge (Fig. 10).
Easily overlooked in the treatment of NUP is the nutritional counseling during the acute stage. To optimize healing, adequate energy (calories) and protein intakes are critical, along with vitamin and minerals. As part of the treatment of NUP, patients are required to take several medications, often with food. However, the pain of NUP restricts food choices. Consumption of soft foods is ideal but it is challenging for most patients to meet nutritional needs by self-selecting foods that they are able to eat. Consumption of nutritional supplements in the form of “Ensure”, “Boost” or equivalent product will help make certain that energy and nutrient needs are met during healing when it is difficult for a patient to consume their regular meals.
A healthy diet is also important for maintaining oral health post-recovery. Dietary recommendations for bone specific nutrients including calcium and vitamin D for Canada and the United States were published in 1997 by the Institute of Medicine based on gender and age (Table 3).2 The majority of individuals living in North America have intakes of calcium and vitamin D that are below the current dietary recommended intakes (DRIs). This is problematic as calcium intakes below 800mg calcium per day are associated with increased risk of periodontal disease.3
Despite the fact that vitamin D is often referred to as the sunshine vitamin because it can be made in the skin through exposure to sunlight, it is important to recognize that for at least half the year there is insufficient sunshine for Canadians to synthesize sufficient levels of vitamin D. Moreover, it is common to wear sunscreen or protective clothing during times of the year when there is opportunity for our skin to endogenously synthesize vitamin D. It is not surprising that NUP is usually seen in the fall and winter months when exposure to sunlight is minimal.
Ten years has passed since the dietary reference intakes for calcium and vitamin D were established, and during this time, a plethora of recent studies suggest that higher intakes of vitamin D, i.e. an intake of 1000 IU vitamin D per day (25 g vitamin D per day) is required for optimal health.4 Interestingly, some of the data on which this higher intake is based is from a study in which higher levels of serum 25(OH)D are associated with lesser gingivitis and clinical attachment loss.5,6 Furthermore, provision of calcium and vitamin D supplements (500 mg calcium plus 700 I.U. (17.5 g) vitamin D per day)) among older individuals (over 65 years of age) with intakes of calcium and vitamin D below recommended levels has been shown to result in greater tooth retention.7
An individual can achieve the recommended levels of dietary calcium by consuming 3-4 servings of dairy products per day (Table 4). Ideal sources include milk, yogurt, cheese, and preferably
low fat varieties. Abundant sources of vitamin D include milk as it is fortified with vitamin D and salmon (Table 5). If canned salmon is consumed with bones, it serves as a rich source of both calcium and vitamin D (Tables 4 & 5). Because dairy products and “fatty” fish (i.e. salmon, herring, mackerel) tend to be the richest sources of both calcium and vitamin D, specific dietary patterns increase health risks associated with suboptimal intakes of these essential nutrients. In these situations, there are two main options: i. consume foods with added calcium and/or vitamin D such as calcium fortified orange juice, or calcium and vitamin D fortified soy beverage (soy does not naturally contain appreciable levels of calcium or vitamin D) or ii. use of calcium and vitamin D supplements.
Commonly asked questions about using calcium supplements include the form of calcium and dosing schedule. The form of calcium does not significantly affect the bioavailability of calcium, i.e. calcium carbonate, calcium citrate have similar biological effects but may differ in tolerability among individuals. Calcium is most effectively absorbed when taken with meals and at multiple times during the day, and it is also beneficial for calcium to be taken in combination with vitamin D.
As for any nutrient, it is important that individuals recognize that there are maximal levels of calcium and vitamin D that should be consumed. For calcium, a maximum of 2200 mg has been set as the safe upper tolerable limit.2 For vitamin D, the safe upper tolerable limit is 2000 IU/day (or 50 g/day).2 As discussed above, this level may need revising based on newer data and is an active area of discussion among health professionals and researchers.
Consuming fish and fish oils should also be considered for periodontal health as well as overall health. Fish oils are the richest dietary source of long chain omega-3 polyunsaturated fatty acids such as docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA) which have anti-inflammatory properties. Epidemiological studies suggest that cardiovascular disease may, at least in part, result from an inflammatory-mediated process such as periodontal disease,8-11 and the connection between cardiovascular disease and periodontal disease is an active area of research. For healthy individuals (i.e. without existing heart disease), the American Heart Association recommends consuming “fatty” fish at least two times per week for cardiovascular health.
Examples of commonly consumed “fatty” fish include salmon, herring and mackerel. Fish oil capsules are widely available for individuals who do not consume fish. Moreover, increasing intakes of fats from other omega-3 sources, i.e. flaxseed, walnuts as well as flaxseed oil is recommended. Flaxseed is being increasingly incorporated into a wide variety of food products in Canada, which may help individuals to make healthier choices about the types of fats they consume while also increasing intakes of fiber which tend to be lower than ideal. Common food sources of flaxseed include breads, cereals, muffins and pastas.
Achieving and maintaining a healthy weight is also important for oral health. Obesity and obesity-related development of type two diabetes increases an individual’s risk of developing periodontal disease.12-14 Successful weight management includes careful attention to foods consumed (both serving size and quality foods, i.e. type of fat, fiber intake) as well as regular physical activity. The Canada Food Guide was revised in 2007, and now provides customized nutrition guidance based on an individual’s age, sex, and physical activity level (please visit http://www.hc-sc.gc.ca/fn-an/food-guide-aliment/index_e. html). Guidelines for physical activity for optimal health have also been established and are tailored to specific age groups (please visit http://www.hc-sc. gc.ca/hl-vs/physactiv/index_e. html). Following the Canada Food Guide in combination with the Guide to Physical Activity will help to maximize oral and overall health, and likely promote an expeditious recovery.
Dr. Fritz is a certified specialist in Periodontics and is in full-time private practice in Fonthill, Ontario. The focus of his periodontal practice is dental implant therapy, bone and soft tissue reconstruction, and oral medicine.
Dr. Ward is a tenured professor in the Department of Nutritional Sciences, Faculty of Medicine University of Toronto. Her research program is focused on the mechanisms by which phytoestrogens (i.e. isoflavones in soy, lignans in flaxseed) and fatty acids regulate bone metabolism, with the long-term goal of developing dietary strategies that protect against fragility fracture.
Oral Health welcomes this original article.
1.Armitage, G.C., Development of a classification system for periodontal diseases and conditions. Ann. Periodontol., 4, 1, 1999.
2. Food and Nutrition Board, Dietary reference intakes for calcium, phosphorus, magnesium, vitamin D and fluoride. Institute of Medicine, National Academy of Sciences, 2004, www.iom.edu/?id=21381.
3.Nishida, M., et al., Calcium and the risk for periodontal disease. J. Periodontol., 71, 1057, 2000.
4.Bischoff-Ferrari, H.A., et al., Estimation of optimal serum concentrations of 25-hydroxyvitamin D for multiple health outcomes. Am. J. Clin. Nutr., 84, 18, 2006.
5.Dietrich, T., et al., Association between serum concentrations of 25-hydroxyvitamin D3 and periodontal disease in the US population. Am. J. Clin. Nutr., 80, 108, 2004.
6.Dietrich, T., et al., Association between serum concentrations of 25-hydroxyvitamin D and gingival inflammation. Am. J. Clin. Nutr., 82, 575, 2005.
7.Krall, E.A., et al., Calcium and vitamin D supplements reduce tooth loss in the elderly. Am. J. Med., 111, 452, 2001.
8.Beck, J.D., et al., Relationship of periodontal disease to carotid artery intima-media wall thickness: the atherosclerosis risk in communities (ARIC) study. Arterioscler. Thromb. Vasc. Biol., 21, 1816, 2001.
9.Demmer, R.T., and Desvarieux, M., Periodontal infections and cardiovascular disease: the heart of the matter. J. Am. Dent. Assoc., 137, 14S, 2006.
10.DeStefano, F., et al., Dental disease and risk of coronary heart disease and mortality. Brit. Med. J., 306, 688, 1993.
11.Mattila, K.J., et al. Dental infections and coronary atherosclerosis. Atherosclerosis. 103, 205, 1993.
12.Genco, R.J., et al., A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J. Periodontol., 76, 2075, 2005.
13.Lim, L.P., et al., Relationship between markers of metabolic control and inflammation on severity of periodontal disease in patients with diabetes mellitus. J. Clin. Periodontol., 34, 118, 2007.
14.Faria-Almeida, R., Navarro, A., Bascones, A., Clinical and metabolic changes after conventional treatment of type 2 diabetic patients with chronic periodontitis. J. Periodontol., 77, 591, 2006.
Clinical Features of NUP
* Unmistakable fetid oris
* Patient feels ill
* Local trauma to area
* Usually teenagers or young adults
* Usually smokers
* Several interdental papillae involved
* Fiery red gingiva
* Papillae “punched out”, ulcerated and covered with a grayish pseudomembrane
* Removal of the membrane reveals bloody raw surface
* Painful lymphadenitis
* Poor nutritional status
* Poor oral hygiene
Differential diagnosis of NUP
* Agranulocytosis, acut
* Benign mucosal pemphigoid
* Herpetic gingivostomatitis
* Syphilitic gingivitis
* Carcinoma and tuberculous ulcers
* Gingival changes resulting from cytostatic or immunosuppressive therapy
* Papillary necrosis after intraligamentary anaesthesia
Dietary reference intakes for calcium and vitamin D, age 31 and older*
|Gender||Age(years)||Calcium(mg/day)||Vitamin D(IU/day or g/day)|
|Females||31-50||1000||200 or 5|
|51-70||1200||400 or 10|
|>70||1200||600 or 15|
|Males||31-50||1000||200 or 5|
|51-70||1200||400 or 10|
|>70||1200||600 or 15|
* Please note that dietary references intakes for calcium and vitamin D for other age groups and stages of the life cycle, including pregnancy and lactation, can be found at http://www.iom.edu/?id=21381
Source: Food and Nutrition Board, Institute of Medicine, National Academy of Sciences, 2004, http://www.iom.edu/?id=21381
Calcium content of selected foods*
|Food(serving size)||Calcium(mg)||# servings/day to meet requirement of 1200 mg(Calcium/day**)|
|Milk — skim, 1%, 2% or whole(1 cup or 250 mL)||~300||~4|
|Yogurt — nonfat, fruit or plain (175 g)||~250-295||~4-5|
|Cheddar cheese(3 cm cube)||~245||~5|
|Salmon with bones, canned(1/2 can)||~240||~5|
|Fortified soy beverage(1 cup or 250 mL)||~300||~4|
|Fortified orange juice(1 cup or 250 mL)||~300||~4|
* This list provides some examples of foods that contain substantial levels of calcium, and by no means is this list exhaustive. For a more extensive list of calcium content of foods, please visit http://www.osteoporosis.ca.
** 1200 mg calcium/day is the recommended intake of calcium for men and women over age 50. http://www.iom.edu/?id=21381
Vitamin D content of selected foods*
|Food(serving size)||Vitamin D(IU or ug)||# servings/day to meet arequirement of 400 IU or(10 g vitamin D/day**)|
|Milk – skim, 1%, 2% or whole(1 cup or 250 mL)||~100 or 2.5||~4|
|Salmon, cooked (100 g)||~360 or 9.0||~1-2|
|Mackerel, cooked (100 g)||~345 or 8.6||~1-2|
|Tuna, canned in oil (100 g)||~200 or 5.0||~2|
* This list provides some examples of foods that contain substantial levels of vitamin D, and by no means is this list exhaustive (please also visit http://ods.od.nih.gov/factsheets/vitamind.asp).
** 400 IU or 10 mg vitamin D/day is the recommended intake of vitamin D for men and women between 51 and 70 years of age. http://www.iom.edu/?id=21381