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Cigarette smoking and oral lesions other than cancer
Cigarette Smoking and Oral Lesions Other Than Cancer STEPHEN J. MERAW, DDS INDRA Z. MUSTAPHA, DDS ROY S. ROGERS III, MD
T
he oral effects of cigarette smoking, as well as the use of other forms of tobacco, have been noted for the past half century.1,2 Growing epidemiologic data has reinforced the clinical correlation between tobacco use and an increased rate of tooth loss3– 6 as well as an increased prevalence and severity of periodontal disease.7 The adverse effects of cigarette smoking on the oral cavity are varied and impact all oral tissue types including gingival, mucosal, and dental. Likewise, the tissues of the oral cavity are affected by other forms of tobacco such as smokeless tobacco, or “chew” tobacco. Recent studies have found smoking to be one of the most significant risk factors in the progression of periodontal disease.8 –11 In the United States alone, 80% of all adults are affected with some form of periodontal disease,12 with greater than a quarter of the adult population smoking cigarettes.13 Thus, it is very likely that most clinicians will encounter periodontal disease in the oral examinations of their patients. The effects of cigarette smoking upon oral health are numerous and vary among individuals. We describe the major effects other than cancer that are attributed to cigarette smoking and tobacco use. These effects include those involving gingival tissue, mucosal tissue, dental tissues, as well as noncancer oral lesions associated with the use of smokeless tobacco, as well as some cultural variants of tobacco use.
Gingival Health Alterations in gingival health associated with smoking vary among individuals. Gingival tissue is that tissue which immediately surrounds a tooth and is contiguous with the tooth and the mucosal tissues. The gingivae consist of fibrous investing tissue covered by keratinized epithelium. Gingival effects include acute necrotizing ulcerative gingivostomatitis, gingivitis and periodontitis, altered gingival healing response, and gingival pigmentary changes.14,15 From Departments of Dentistry and Dermatology, Mayo Clinic and Mayo Foundation, Rochester, Minnesota. Address correspondence to Dr. Roy S. Rogers III, Department of Dermatology, Mayo Clinic, 200 First St. SW, Rochester, MN 55905-0001. © 1998 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010
Smoking and Gingivitis and Periodontitis Pindborg demonstrated an association between the prevalence of acute ulcerative gingivitis and smoking as early as 1946.1 Acute necrotizing ulcerative gingivitis (ANUG, Vincent’s disease, trench mouth) is a painful inflammatory condition of acute gingivitis characterized by ulceration and necrosis of the gingival margin and destruction of the interdental papilla (Fig 1). It is initiated by bacterial antigens and maintained by the host response to those antigens. Although the mechanism of interaction with smoking is not fully understood, smoking has been shown to have a strong correlation with ANUG,1,2 with the stereotypical patient presenting as a young smoker.16 It has been suggested that cigarette smoking may have a dual role in the pathogenesis of this condition, both in terms of a local effect and a systemic effect.16 Locally, it has been suggested that the tar and other by-products of combustion serve as deposits on the tooth surface that aid in the accumulation of plaque and bacteria, which in turn are irritants for the gingiva. Systemically, it has been suggested that the effects of nicotine as a sympathomimetic drug and chemoattractant also aid in the progression of this condition. Increased awareness regarding the role of tobacco use and the prevalence and severity of periodontal diseases and subsequent tooth loss has arisen through many studies over the past two decades.3–7 Although the pathogenesis of gingivitis and periodontitis is viewed as bacterially elicited inflammation of the marginal gingiva and disease of the tooth-supporting apparatus, respectively, smoking has been shown repeatedly to have a strong positive correlation with a more pronounced effect of both of these conditions.10,16,17 In considering the effects of smoking upon the pathogenesis and progression of periodontitis, one must realize the multiple factors that play a role in the initiation and progression of periodontitis. These factors include host resistance, bacterial pathogenicity, oral hygiene effectiveness, as well as the presence of local factors that aid in accumulation of bacterial plaque. The exact role that smoking plays in each of these factors is not fully known; however, this is an area of 0738-081X/98/$19.00 PII S0738-081X(98)00048-0
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posttherapy periodontal pocketing30,31 and less gain in clinical attachment following periodontal pocket reduction surgery over time.31 Likewise, soft-tissue grafting procedures have been shown to exhibit a poorer success rate.32 These considerations should be discussed with smokers when recommending surgical therapy, or when discussing goals or expected outcome.
Smoking and Pigmentary Changes of the Gingiva
Figure 1. Acute necrotizing ulcerative gingivitis. Note the ulceration of the gingival margin and destruction of the interdental papilla.
active investigation. It is thought that smoking alters the host response by impairing normal host immunity in neutralizing infection.18 Smokers have been shown to have decreased levels of salivary IgA antibodies19 and serum IgG antibodies to known periodontopathogens such as Prevotella intermedia and Fusobacterium nucleatum.19 Additionally, smoking has been shown to have adverse effects upon neutrophil function,20 –22 which is important in host response to infection. Other considerations include the effects of nicotine, which has been shown to suppress the proliferation of cultured osteoblasts,23 potentially affecting the reparative and regenerative potential, as well as possibly reducing gingival blood flow.24 Smoking affects the periodontal ecosystem. Smokers have been shown to have more anaerobic periodontal pockets,25 which are usually associated with periodontal disease. Studies have not been conclusive, however, as to whether this effect of altering the microbial makeup of the periodontal flora from smoking adversely affects the periodontal tissues. Other characteristics of smokers relevant to periodontal disease from an epidemiologic standpoint include increased calculus formation,26 which can accelerate the accumulation of bacterial plaque locally; greater supporting bone loss,27,28 which can compromise the health of the tooth; and greater prevalence of deep pockets,27,28 which can further accumulate microbes and their toxins. All of these factors add up to a great disadvantage to the smoker in terms of the pathogenesis and progression of periodontal disease. There is a significant difference between smokers and nonsmokers with respect to response to therapy and long-term prognosis with therapy of periodontal disease. It has been shown that greater than 90% of refractory periodontitis patients, or those patients who have persistent disease following treatment, are smokers.29 Other considerations include significantly deeper
Abnormal smoking-induced pigmentation, or smokingassociated melanosis, may occur in the gingival tissues, and most commonly presents in the anterior labial gingiva.33 Although this condition is benign, patients may have esthetic concerns. Smoker’s melanosis can mask other lesions. The pathogenesis is stimulation of melanocyte function by some component of cigarette smoke.33 There is increased melanin production resulting in pigmentation of basal keratinocytes.33 This pigmentation is histologically similar to physiologic pigmentation. A return to normal pigmentation occurs with smoking cessation with gradual improvement over several months to years.33
Mucosal Health Benign mucosal alterations are likely to manifest clinically and histologically in those who smoke. Obvious locations such as the palate and tongue may be affected, but any location in the oral cavity can be subject to mucosal changes. An understanding of benign conditions of the oral mucosa helps the practitioner realize which ones may have the potential to undergo malignant transformation. Such precancerous lesions should be confronted with a high index of suspicion. Thus, frequent intraoral exams are necessary for smokers despite the absence of symptoms.
Nicotine Stomatitis Pipe and cigar smokers often present with benign palatal lesions found posterior to the rugae known as nicotine stomatitis or leukokeratosis nicotini palati. The etiology may be the trauma of heat or chemical irritants in tobacco.34 Clinically multiple discrete keratotic papules with depressed red centers are noted on examination. These represent dilated and inflamed minor salivary gland duct openings (Fig 2). As the irritation persists, the clinical picture of nicotine stomatitis progressively changes from red to grayish-white owing to reactive hyperkeratosis. Each papule remains discrete, giving a characteristic cobblestone or parboiled appearance.34 Histologically, hyperkeratosis and parakeratosis of the palate imparts a whitish appearance. Edema, infiltration by plasma cells in the connective tissue, and plugging of ductal lumina create the characteristic palatal papules. Malignant transformation does not occur
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Figure 2. Nicotinic stomatitis. Note the keratotic papules giving a cobblestone appearance.
in nicotine stomatitis but has been seen in reverse smokers (see below).35 The differential diagnosis includes palatal papillary hyperplasia, denture stomatitis, and atrophic candidiasis.36 All three conditions, unlike nicotine stomatitis, develop under a denture. In addition, atrophic candidiasis is easily identified by culture. A history of smoking helps exclude other lesions. Discontinuance of smoking results in regression of nicotine stomatitis.
Reverse Smoking and Palatal Mucosal Changes The habit of reverse smoking is practiced in various parts of the world such as the Indian subcontinent and the Philippines. In rural villages of India, for example, one method of smoking tobacco is the “chutta,” which can be smoked both conventionally and reversed. In reverse smoking, the lit end is held inside the mouth. The majority of reverse smokers exhibit palatal changes including leukoplakia, mucosal thickening, fissuring, pigmentation, nodularity, erythema, and ulceration.37 Research data from Asian studies implicates reverse smoking with significantly more palatal lesions than conventional smoking.38 Oral squamous cell carcinoma may develop with the chronic lesions of reverse smoking.
Smoking and the Tongue Hypertrophy of the filiform papillae and retardation of the normal rate of desquamation on the dorsal surface of the tongue produce a hair-like appearance (hairy tongue, black hairy tongue). These lesions have been associated with heavy smoking. The etiology is multifactorial and may include smoking, antibiotic treatment, systemic corticosteroid therapy, oxygenating mouth rinses, or radiation therapy for head and neck malignancies.39 The hairy tongue may also be related to changes in oral pH with alterations in microbial flora. Attempts to culture specific pathogens have yielded inconsistent results.39
Figure 3. Black hairy tongue. Note the hair-like appearance due to elongation of the filiform papillae.
Clinically, the hairy tongue may begin near the foramen cecum and spread anteriorly and laterally. The elongated filiform papilla may be several millimeters in length and their color may range from white to brown or black (Fig 3). Color changes occur because of intrinsic stains from chromogenic microorganisms or extrinsic stains from food or tobacco. Individuals are usually asymptomatic, but they may report a gagging or tickling sensation if the papillae become particularly long. For most, the concern is cosmetic, especially when the patient has a black hairy tongue. A biopsy is usually not necessary for diagnosis due to the typical presentation. Treatment consists of brushing or scraping of the tongue and improving oral hygiene. Often, removing some or all of the predisposing factors enhances resolution of this problem.
Smoking and Leukoplakia Leukoplakia is a term used to designate a clinically white patch or plaque on the oral mucosa that cannot be removed by scraping and cannot be classified clinically or microscopically as any other disease entity40 (Fig 4). It usually represents a benign hyperkeratotic process most frequently related to tobacco use or trauma. Leukoplakia is usually asymptomatic and is often discovered by routine exam. Any location in the oral cavity may be affected. Leukoplakia is a significant clinical finding because it represents a premalignant lesion. When the trauma is removed, the keratotic process may or may not reverse itself.40 All leukoplakias that do not clear after removal of traumatic predisposing factors should be followed by
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Figure 4.
Leukoplakia of the labial mucosa.
periodic exams. A biopsy is indicated to classify the risk of malignant transformation. If severe dysplasia is present histologically, the lesion should be surgically removed. For those patients with mild or moderate dysplasia, periodic examinations at 3- to 6-month intervals should be carried out. Repeat biopsies may be necessary. Erythroleukoplakia is leukoplakia that clinically has a red or erythematous component. Such lesions have been found to be more likely to undergo dysplastic or malignant changes.40 Silverman and colleagues reported on a 1984 study that showed a fourfold increased risk of carcinoma present in erythroplastic lesions.41 All mucosal lesions with an erythroplastic component should be treated with a high index of suspicion; each should be studied histologically, and the patient should be followed very closely.
Dental Health Changes in the health of the dentition, or alterations in dental architecture due to smoking, may impact only one, or several teeth, or create occlusal disharmony. Changes in the tooth structure from smoking include staining or abrasion. Developmental or congenital effects of smoking by the pregnant mother while the tooth is developing are currently unknown. In addition to the odontogenic tissue itself, smoking has been shown to effect the supporting bone of the tooth.42– 44 This has been particularly relevant when a treatment plan calling for extraction of the tooth and/or replacement with an endosseous dental implant is considered. Smokers have shown significantly different results from nonsmokers with respect to dental implants.
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Figure 5. Extrinsic staining, calculus, and periodontal disease. Note the dark staining due to smoking deposits and the exposed root surfaces due to periodontal disease.
(Fig 5). These stains are generally of esthetic concern only; however, they may aid in the accumulation of plaque.15 Treatment generally consists of dental prophylaxis with mild abrasives that should remove the extrinsic stains; however, the stains will quickly reappear with continued smoking. Abrasion is the pathologic wearing of the teeth from an abrasive substance and/or destructive habit.45 While cigarette smoking is usually not associated with abrasion, other forms of tobacco use such as pipe smoking or smokeless tobacco are common causes. One of the concerns regarding abrasion is the point at which the loss of dental structure exposes the dental pulp, resulting in the need for root canal therapy (Fig 6). Corrective action in terms of stopping the destructive habit, or crown restorations of the affected occluding teeth, may be warranted in more severe cases to prevent pulpal injury. More severe abrasion may result in alteration of the patient’s occlusion causing disharmony such as an anterior open bite or apertognathia (Fig 7). Apertognathia develops in pipe smokers and usually occurs unilaterally on the smoker’s favorite side. Treatment would
Smoking and Staining, Abrasion, and Malocclusion Smoking may be one of several ways to acquire extrinsic or exogenous staining of the teeth. Tar and other by-products of combustion become deposits on the tooth surface, which usually appear as dark brown to black discoloration on the cervical aspect of the tooth45
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Figure 6.
Dental abrasion.
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Figure 7. Apertognathia secondary to pipe smoking. This patient had been a pipe smoker for many years.
generally consist of crown restorations of the occluding teeth.
Smoking and Alveolar Osteitis Alveolar osteitis or “dry socket” is a potential complication of tooth extraction, particularly of mandibular third molars.43,44 Although the etiology is still not fully understood, it has a prevalence from 2.6% to 11% in nonsmokers.42,43 This condition usually presents as a severe, throbbing pain in the alveolus of the surgical site for 2 or more days postoperatively.42 Denuded bone, odor, or a greyish exudate may be present at the site.42 Studies have shown a significant difference in the incidence of alveolar osteitis between smokers and nonsmokers, with nonsmokers having an incidence from two43 to four and a half times higher42 than that of nonsmokers. Treatment generally consists of daily packing of the alveolus with a eugenol dressing until symptoms disappear, as this condition is not responsive to systemic analgesics alone.42
Smoking and Dental Implants The use of endosseous dental implants for tooth replacement of edentulous areas has become a more widely used and predictable practice. The achievement of integration of the dental implant with the alveolar bone, or osseointegration, is the primary goal following placement of the implant. Failure rates of this process are generally under 10% in nonsmokers,46 but have been shown to be over seven times higher in smokers than in nonsmokers.47 Although the relationship of smoking to the adverse effects on osseointegration is poorly understood, smokers have been shown to have lower bone density than nonsmokers.48 This is a primary predisposing factor for implant failure. The benefits of smoking cessation for as little as 9 weeks during implant healing has been shown to be significant with respect to implant osseointegration.47 Smokers should be cautioned regarding higher failure rates when this type of treatment is planned.
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Figure 8. Snuff keratosis. Note the gingival recession, mucosal changes, and remnants of smokeless tobacco.
Smokeless Tobacco and the Oral Mucosa There are three forms of smokeless tobacco used in the United States: moist snuff, chewing tobacco, and dry snuff. Moist snuff is the most common form of smokeless tobacco used in the United States today. It is made with moist, finely ground tobacco. Snuff is tucked or “dipped” between the gingiva and the lip or cheek. A second form is chewing tobacco consisting of shredded tobacco, which is sold either loose, in a bar, or as a “plug.” Synonymous names are “wad,” “quid,” “twist,” or “chaw.” Often, a golfball sized amount is placed in the cheek and sucked or chewed. Dry snuff is inhaled powdered tobacco. Dry snuff is used infrequently in the United States. Smokeless tobacco is also used in other parts of the world. It is used commonly in many regions in Asia. Here, smokeless tobacco is consumed in the forms of “nass,” “naswar,” and “pan.” Each year, 10 million to 16 million Americans use smokeless tobacco, with annual sales exceeding a billion dollars.49 Its use is increasing among young people in this country. The CDC analyzed data from a 1995 Youth Risk Behavior Survey and found an increasing prevalence in smokeless tobacco use among high school students 18 years of age and younger.50
Adverse Effects of Smokeless Tobacco The 1994 Report of the Surgeon General concluded that use of smokeless tobacco “can cause gingival recession, periodontal destruction and cancer of the mouth.”51 An oral lesion uniquely characteristic to smokeless tobacco users is “snuff dipper’s patch,” also called “tobacco chewer’s lesion” and “snuff keratosis” (Fig 8). Snuff dipper’s patch occurs in areas corresponding to the intraoral placement of the smokeless tobacco. The National Health and Nutrition Examination Survey has classified this lesion into one of three degrees according to its progression or severity.52
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Degree 1 lesions present with normal color to pale white or gray. Slight superficial wrinkling of the mucosa exists but may disappear upon manually stretching this tissue. The oral mucosa does not appear thickened. A Degree 2 lesion has undergone a distinct whitish-gray or an occasionally red color change. Obvious wrinkles are seen but the mucosa is still not thickened. The color change remains upon stretching of the lesion. Degree 3 lesions possess thickened oral mucosa with deep furrows in the surface epithelium. The mucosa remains whitish-gray and may also have red areas. This lesion persists when stretched. Treatment consists of tobacco-use cessation upon which resolution of the mucosal alterations are likely. If regression to normal appearance does not begin within 14 days, biopsy and histological evaluation are warranted. Close follow-up is in order owing to the precancerous nature of these lesions.
Conclusions It has been well recognized that tobacco can induce changes in the gingiva, oral mucosa, and dentition. Careful history taking can identify smoking or tobacco use as a risk factor in patients with periodontal disease. Not only are these individuals more susceptible to periodontal disease, but smokers also have a poorer response to dental therapies. Thorough clinical examination can reveal the detrimental effects that tobacco has on the teeth and oral mucosa. Cessation of the habit may stop the progression of ill effects on the oral cavity. The adverse effects may be completely preventable in those who never use tobacco. Precancerous lesions merit special concern for both the health professional and the patient. Most benign lesions respond favorably to cessation of the habit. It is uncertain, though, which lesions will undergo dysplastic or malignant transformation. It is also important to note that not all cancerous conditions are preceded by benign lesions. For these reasons, tobacco use necessitates periodic, complete intraoral exams.
References 1. Pindborg JJ. Tobacco and gingivitis: I. Statistical examination of the significance of tobacco in the development of ulceromembranous gingivitis and in the formation of calculus. J Dent Res 1947;26:261– 4. 2. Pindborg JJ. Tobacco and gingivitis: II. Correlation between consumption of tobacco, ulceromembranous gingivitis and calculus. J Dent Res 1949;28:460 –3. 3. Ahlquist M, Bengtsson C, Hollender L, et al. Smoking habits and tooth loss in Swedish women. Community Dent Oral Epidemiol 1989;17:144 –7. ¨ sterberg T, Mellstro¨m D. Tobacco smoking: A major risk 4. O factor for loss of teeth in three 70-year-old cohorts. Community Dent Oral Epidemiol 1986;14:367–70.
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5. Holm G. Smoking as an additional risk for tooth loss. J Periodontol 1994;65:996 –1001. ´ lafsson SH. Tobacco smok6. Ragnarsson E, Elı´asson ST, O ing, a factor in tooth loss in Reykjavı´k, Iceland. Scand J Dent Res 1992;100:322– 6. 7. Haber J, Wattles J, Crowley M, et al. Evidence for cigarette smoking as a major risk factor for periodontitis. J Periodontol 1993;64:16 –23. 8. Bartecchi CE, MacKenzie TD, Schrier RW. The human costs of tobacco use: I. N Engl J Med 1994;331:907–12. 9. Grossi SG, Zambon JJ, Ho AW, et al. Assessment of risk for periodontal disease: I. Risk indicators for attachment loss. J Periodontol 1994;65:260 –7. 10. Grossi SG, Genco RJ, Machtei EE, et al. Assessment of risk for periodontal disease: II. Risk indicators for alveolar bone loss. J Periodontol 1995;66:23–9. 11. Locker D, Leake JL. Risk indicators and risk markers for periodontal disease experience in older adults living independently in Ontario, Canada. J Dent Res 1993;72:9 –17. 12. U.S. Public Health Service, National Institute of Dental Research. Oral health of United States adults: National findings (NIH Publication No. 87-2868). Bethesda, MD: NIDR, 1987. 13. Centers for Disease Control and Prevention. MMWR April 2, 1993;42:230 –2. 14. Lindhe J. Textbook of clinical periodontology. Copenhagen: Munksgaard, 1983:19 – 66. 15. Rateitschak KM, Rateitschak EM. Color atlas of dental medicine: Vol 1. Periodontology. New York: Thieme Medical Publishers, 1989:49 –51. 16. Preber H, Kant T, Bergstrom J. Cigarette smoking, oral hygiene and periodontal health in Swedish army conscripts. J Clin Periodontol 1980;7:106 –13. 17. Haber J. Cigarette smoking: A major risk factor for periodontitis. Compendium Cont Educ Dent 1994;15:1002–14. 18. Seymour GJ. Importance of the host response in the periodontium. J Periodontol 1991;18:421– 6. 19. Bennet KR, Read PC. Salivary immunoglobin A levels in normal subjects, tobacco smokers, and patients with minor aphthous ulceration. Oral Surg Oral Med Oral Pathol 1982;53:461–5. 20. Kenney EG, Kraal JH, Saxe SR, et al. The effect of cigarette smoking on human oral polymorphonuclear leukocytes. J Periodontol Res 1977;12:227–34. 21. Codd EE, Swim AT, Bridges RB. Tobacco smokers’ neutrophils are desensitized to chemotactic peptide-stimulated oxygen uptake. J Lab Clin Med 1987;110:648 –52. 22. Lannan S, McLean A, Drost E, et al. Changes in neutrophil morphology and morphometry following exposure to cigarette smoke. Int J Exp Pathol 1992;73:183–91. 23. Fang MA, Frost PJ, Iida-Klein A, et al. Effects of nicotine on cellular function in UMR 106-01 osteoblast-like cells. Bone 1991;12:283– 6. 24. Clarke NG, Shephard BC, Hirsch RS. The effects of intraarterial epinephrine and nicotine on gingival circulation. Oral Surg Oral Med Oral Pathol 1981;52:577– 82. 25. Kenney EB, Saxe SR, Bowles RD. The effect of cigarette smoking on anaerobiosis in the oral cavity. J Periodontol 1975;46:82–5. 26. Position Paper. Tobacco use and the periodontal patient.
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American Academy of Periodontology. J Periodontol 1996;67:51– 6. Solomon HA, Prior RL, Bross ID. Cigarette smoking and periodontal disease. J Am Dent Assoc 1968;77:1081– 4. Bergstro¨m J, Floderus-Myrhed B. Co-twin control study of the relationship between smoking and some periodontal disease factors. Community Dent Oral Epidemiol 1983;11: 113– 6. MacFarlane GD, Herzberg MC, Wolff LF, et al. Refractory periodontitis associated with abnormal polymorphonuclear leukocyte phagocytosis and cigarette smoking. J Periodontol 1992;63:908 –13. Preber H, Bergstro¨m J. Effect of cigarette smoking on periodontal healing following surgical therapy. J Clin Periodontol 1990;17:324 – 8. Ah MKB, Johnson GK, Kaldahl WB, et al. The effect of smoking on the response to periodontal therapy. J Clin Periodontol 1994;21:91–7. Miller PD Jr. Root coverage with the free gingival graft: factors associated with incomplete coverage. J Periodontol 1987;58:674 – 81. Regazi JA, Sciubba J. Oral pathology: Clinical-pathologic correlations. 2nd ed. Philadelphia: Saunders, 1993:162–3. Langlais RP, Miller CS. Color atlas of common oral disease. Philadelphia: Lea and Febiger, 1992:55–7. Regazi JA. Oral pathology: Clinical-pathologic conditions. Philadelphia: Saunders, 1989;93:102–104. Wood NK, Goaz PW. Differential diagnosis of oral lesions. St. Louis, MO: Mosby-Yearbook, 1991;8:124 –5. Mercado-Ortiz G, Wilson D, Jiang DJ. Reverse smoking and palatal changes in Filipino women: Epidemiologic features. Aust Dent J 1996;41:300 –3. Silverman S, Shillitoe EJ. Oral cancer. Atlanta: American Cancer Society, 1990;2:12–15. Regazi JA. Oral pathology: Clinical-pathologic conditions. Philadelphia: Saunders, 1989:102–3. Silverman S, Shillitoe EJ. Oral cancer. Atlanta: American Cancer Society, 1990;2:14 – 6.
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41. Silverman S, Gorsky M, Lozada F. Oral leukoplakia and malignant transformation: A follow-up study of 257 patients. Cancer 1984;53:563– 8. 42. Sweet JB, Butler DP. The relationship of smoking to localized osteitis. J Oral Surgery 1979;37:732–5. 43. Bonine FL. Effect of chlorhexidine rinse on the incidence of dry socket in impacted mandibular third molar extraction sites. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995;79:154 – 8. 44. Hooley JR, Golden DP. The effect of polylactic acid granules on the incidence of alveolar osteitis after mandibular third molar surgery: A prospective randomized study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995; 80:279 – 83. 45. Regazi JA, Sciubba J. Oral pathology: Clinical-pathologic correlations. 2nd ed. Philadelphia: Saunders, 1993:500 –1. 46. Albrektsson T, Dahl E, Enbom L, et al. Osseointegrated oral implants. Swedish multicenter study of 8,139 consecutively inserted Nobelpharma implants. J Periodontol 1988;57:287–96. 47. Bain CA. Smoking and implant failure— benefits of a smoking-cessation protocol. Int J Oral Maxillofac Implants 1996;11:756 –9. 48. Bain CA, Moy PK. The influence of smoking on bone quality and implant failure (Abstract). Int J Oral Maxillofac Implants 1994;9:123. 49. McGowan JM, Ship JA. Fighting the use of smokeless tobacco. J Pract Hygiene 1996;5:29 –32. 50. Anonymous. Tobacco use and usual source of cigarettes among high school students—United States, 1995. MMWR 1996;45(20):413– 8. 51. U.S. Department of Health and Human Services. Preventing tobacco use among young people: A report of the Surgeon General executive summary. Washington, DC: Centers for Disease Control and Prevention, 1994:1–15. 52. National Health and Nutrition Examination Survey: III. Health survey methods. Rockville, MD: Westat, 1984:1– 8.
T
he oral effects of cigarette smoking, as well as the use of other forms of tobacco, have been noted for the past half century.1,2 Growing epidemiologic data has reinforced the clinical correlation between tobacco use and an increased rate of tooth loss3– 6 as well as an increased prevalence and severity of periodontal disease.7 The adverse effects of cigarette smoking on the oral cavity are varied and impact all oral tissue types including gingival, mucosal, and dental. Likewise, the tissues of the oral cavity are affected by other forms of tobacco such as smokeless tobacco, or “chew” tobacco. Recent studies have found smoking to be one of the most significant risk factors in the progression of periodontal disease.8 –11 In the United States alone, 80% of all adults are affected with some form of periodontal disease,12 with greater than a quarter of the adult population smoking cigarettes.13 Thus, it is very likely that most clinicians will encounter periodontal disease in the oral examinations of their patients. The effects of cigarette smoking upon oral health are numerous and vary among individuals. We describe the major effects other than cancer that are attributed to cigarette smoking and tobacco use. These effects include those involving gingival tissue, mucosal tissue, dental tissues, as well as noncancer oral lesions associated with the use of smokeless tobacco, as well as some cultural variants of tobacco use.
Gingival Health Alterations in gingival health associated with smoking vary among individuals. Gingival tissue is that tissue which immediately surrounds a tooth and is contiguous with the tooth and the mucosal tissues. The gingivae consist of fibrous investing tissue covered by keratinized epithelium. Gingival effects include acute necrotizing ulcerative gingivostomatitis, gingivitis and periodontitis, altered gingival healing response, and gingival pigmentary changes.14,15 From Departments of Dentistry and Dermatology, Mayo Clinic and Mayo Foundation, Rochester, Minnesota. Address correspondence to Dr. Roy S. Rogers III, Department of Dermatology, Mayo Clinic, 200 First St. SW, Rochester, MN 55905-0001. © 1998 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010
Smoking and Gingivitis and Periodontitis Pindborg demonstrated an association between the prevalence of acute ulcerative gingivitis and smoking as early as 1946.1 Acute necrotizing ulcerative gingivitis (ANUG, Vincent’s disease, trench mouth) is a painful inflammatory condition of acute gingivitis characterized by ulceration and necrosis of the gingival margin and destruction of the interdental papilla (Fig 1). It is initiated by bacterial antigens and maintained by the host response to those antigens. Although the mechanism of interaction with smoking is not fully understood, smoking has been shown to have a strong correlation with ANUG,1,2 with the stereotypical patient presenting as a young smoker.16 It has been suggested that cigarette smoking may have a dual role in the pathogenesis of this condition, both in terms of a local effect and a systemic effect.16 Locally, it has been suggested that the tar and other by-products of combustion serve as deposits on the tooth surface that aid in the accumulation of plaque and bacteria, which in turn are irritants for the gingiva. Systemically, it has been suggested that the effects of nicotine as a sympathomimetic drug and chemoattractant also aid in the progression of this condition. Increased awareness regarding the role of tobacco use and the prevalence and severity of periodontal diseases and subsequent tooth loss has arisen through many studies over the past two decades.3–7 Although the pathogenesis of gingivitis and periodontitis is viewed as bacterially elicited inflammation of the marginal gingiva and disease of the tooth-supporting apparatus, respectively, smoking has been shown repeatedly to have a strong positive correlation with a more pronounced effect of both of these conditions.10,16,17 In considering the effects of smoking upon the pathogenesis and progression of periodontitis, one must realize the multiple factors that play a role in the initiation and progression of periodontitis. These factors include host resistance, bacterial pathogenicity, oral hygiene effectiveness, as well as the presence of local factors that aid in accumulation of bacterial plaque. The exact role that smoking plays in each of these factors is not fully known; however, this is an area of 0738-081X/98/$19.00 PII S0738-081X(98)00048-0
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posttherapy periodontal pocketing30,31 and less gain in clinical attachment following periodontal pocket reduction surgery over time.31 Likewise, soft-tissue grafting procedures have been shown to exhibit a poorer success rate.32 These considerations should be discussed with smokers when recommending surgical therapy, or when discussing goals or expected outcome.
Smoking and Pigmentary Changes of the Gingiva
Figure 1. Acute necrotizing ulcerative gingivitis. Note the ulceration of the gingival margin and destruction of the interdental papilla.
active investigation. It is thought that smoking alters the host response by impairing normal host immunity in neutralizing infection.18 Smokers have been shown to have decreased levels of salivary IgA antibodies19 and serum IgG antibodies to known periodontopathogens such as Prevotella intermedia and Fusobacterium nucleatum.19 Additionally, smoking has been shown to have adverse effects upon neutrophil function,20 –22 which is important in host response to infection. Other considerations include the effects of nicotine, which has been shown to suppress the proliferation of cultured osteoblasts,23 potentially affecting the reparative and regenerative potential, as well as possibly reducing gingival blood flow.24 Smoking affects the periodontal ecosystem. Smokers have been shown to have more anaerobic periodontal pockets,25 which are usually associated with periodontal disease. Studies have not been conclusive, however, as to whether this effect of altering the microbial makeup of the periodontal flora from smoking adversely affects the periodontal tissues. Other characteristics of smokers relevant to periodontal disease from an epidemiologic standpoint include increased calculus formation,26 which can accelerate the accumulation of bacterial plaque locally; greater supporting bone loss,27,28 which can compromise the health of the tooth; and greater prevalence of deep pockets,27,28 which can further accumulate microbes and their toxins. All of these factors add up to a great disadvantage to the smoker in terms of the pathogenesis and progression of periodontal disease. There is a significant difference between smokers and nonsmokers with respect to response to therapy and long-term prognosis with therapy of periodontal disease. It has been shown that greater than 90% of refractory periodontitis patients, or those patients who have persistent disease following treatment, are smokers.29 Other considerations include significantly deeper
Abnormal smoking-induced pigmentation, or smokingassociated melanosis, may occur in the gingival tissues, and most commonly presents in the anterior labial gingiva.33 Although this condition is benign, patients may have esthetic concerns. Smoker’s melanosis can mask other lesions. The pathogenesis is stimulation of melanocyte function by some component of cigarette smoke.33 There is increased melanin production resulting in pigmentation of basal keratinocytes.33 This pigmentation is histologically similar to physiologic pigmentation. A return to normal pigmentation occurs with smoking cessation with gradual improvement over several months to years.33
Mucosal Health Benign mucosal alterations are likely to manifest clinically and histologically in those who smoke. Obvious locations such as the palate and tongue may be affected, but any location in the oral cavity can be subject to mucosal changes. An understanding of benign conditions of the oral mucosa helps the practitioner realize which ones may have the potential to undergo malignant transformation. Such precancerous lesions should be confronted with a high index of suspicion. Thus, frequent intraoral exams are necessary for smokers despite the absence of symptoms.
Nicotine Stomatitis Pipe and cigar smokers often present with benign palatal lesions found posterior to the rugae known as nicotine stomatitis or leukokeratosis nicotini palati. The etiology may be the trauma of heat or chemical irritants in tobacco.34 Clinically multiple discrete keratotic papules with depressed red centers are noted on examination. These represent dilated and inflamed minor salivary gland duct openings (Fig 2). As the irritation persists, the clinical picture of nicotine stomatitis progressively changes from red to grayish-white owing to reactive hyperkeratosis. Each papule remains discrete, giving a characteristic cobblestone or parboiled appearance.34 Histologically, hyperkeratosis and parakeratosis of the palate imparts a whitish appearance. Edema, infiltration by plasma cells in the connective tissue, and plugging of ductal lumina create the characteristic palatal papules. Malignant transformation does not occur
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Figure 2. Nicotinic stomatitis. Note the keratotic papules giving a cobblestone appearance.
in nicotine stomatitis but has been seen in reverse smokers (see below).35 The differential diagnosis includes palatal papillary hyperplasia, denture stomatitis, and atrophic candidiasis.36 All three conditions, unlike nicotine stomatitis, develop under a denture. In addition, atrophic candidiasis is easily identified by culture. A history of smoking helps exclude other lesions. Discontinuance of smoking results in regression of nicotine stomatitis.
Reverse Smoking and Palatal Mucosal Changes The habit of reverse smoking is practiced in various parts of the world such as the Indian subcontinent and the Philippines. In rural villages of India, for example, one method of smoking tobacco is the “chutta,” which can be smoked both conventionally and reversed. In reverse smoking, the lit end is held inside the mouth. The majority of reverse smokers exhibit palatal changes including leukoplakia, mucosal thickening, fissuring, pigmentation, nodularity, erythema, and ulceration.37 Research data from Asian studies implicates reverse smoking with significantly more palatal lesions than conventional smoking.38 Oral squamous cell carcinoma may develop with the chronic lesions of reverse smoking.
Smoking and the Tongue Hypertrophy of the filiform papillae and retardation of the normal rate of desquamation on the dorsal surface of the tongue produce a hair-like appearance (hairy tongue, black hairy tongue). These lesions have been associated with heavy smoking. The etiology is multifactorial and may include smoking, antibiotic treatment, systemic corticosteroid therapy, oxygenating mouth rinses, or radiation therapy for head and neck malignancies.39 The hairy tongue may also be related to changes in oral pH with alterations in microbial flora. Attempts to culture specific pathogens have yielded inconsistent results.39
Figure 3. Black hairy tongue. Note the hair-like appearance due to elongation of the filiform papillae.
Clinically, the hairy tongue may begin near the foramen cecum and spread anteriorly and laterally. The elongated filiform papilla may be several millimeters in length and their color may range from white to brown or black (Fig 3). Color changes occur because of intrinsic stains from chromogenic microorganisms or extrinsic stains from food or tobacco. Individuals are usually asymptomatic, but they may report a gagging or tickling sensation if the papillae become particularly long. For most, the concern is cosmetic, especially when the patient has a black hairy tongue. A biopsy is usually not necessary for diagnosis due to the typical presentation. Treatment consists of brushing or scraping of the tongue and improving oral hygiene. Often, removing some or all of the predisposing factors enhances resolution of this problem.
Smoking and Leukoplakia Leukoplakia is a term used to designate a clinically white patch or plaque on the oral mucosa that cannot be removed by scraping and cannot be classified clinically or microscopically as any other disease entity40 (Fig 4). It usually represents a benign hyperkeratotic process most frequently related to tobacco use or trauma. Leukoplakia is usually asymptomatic and is often discovered by routine exam. Any location in the oral cavity may be affected. Leukoplakia is a significant clinical finding because it represents a premalignant lesion. When the trauma is removed, the keratotic process may or may not reverse itself.40 All leukoplakias that do not clear after removal of traumatic predisposing factors should be followed by
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Figure 4.
Leukoplakia of the labial mucosa.
periodic exams. A biopsy is indicated to classify the risk of malignant transformation. If severe dysplasia is present histologically, the lesion should be surgically removed. For those patients with mild or moderate dysplasia, periodic examinations at 3- to 6-month intervals should be carried out. Repeat biopsies may be necessary. Erythroleukoplakia is leukoplakia that clinically has a red or erythematous component. Such lesions have been found to be more likely to undergo dysplastic or malignant changes.40 Silverman and colleagues reported on a 1984 study that showed a fourfold increased risk of carcinoma present in erythroplastic lesions.41 All mucosal lesions with an erythroplastic component should be treated with a high index of suspicion; each should be studied histologically, and the patient should be followed very closely.
Dental Health Changes in the health of the dentition, or alterations in dental architecture due to smoking, may impact only one, or several teeth, or create occlusal disharmony. Changes in the tooth structure from smoking include staining or abrasion. Developmental or congenital effects of smoking by the pregnant mother while the tooth is developing are currently unknown. In addition to the odontogenic tissue itself, smoking has been shown to effect the supporting bone of the tooth.42– 44 This has been particularly relevant when a treatment plan calling for extraction of the tooth and/or replacement with an endosseous dental implant is considered. Smokers have shown significantly different results from nonsmokers with respect to dental implants.
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Figure 5. Extrinsic staining, calculus, and periodontal disease. Note the dark staining due to smoking deposits and the exposed root surfaces due to periodontal disease.
(Fig 5). These stains are generally of esthetic concern only; however, they may aid in the accumulation of plaque.15 Treatment generally consists of dental prophylaxis with mild abrasives that should remove the extrinsic stains; however, the stains will quickly reappear with continued smoking. Abrasion is the pathologic wearing of the teeth from an abrasive substance and/or destructive habit.45 While cigarette smoking is usually not associated with abrasion, other forms of tobacco use such as pipe smoking or smokeless tobacco are common causes. One of the concerns regarding abrasion is the point at which the loss of dental structure exposes the dental pulp, resulting in the need for root canal therapy (Fig 6). Corrective action in terms of stopping the destructive habit, or crown restorations of the affected occluding teeth, may be warranted in more severe cases to prevent pulpal injury. More severe abrasion may result in alteration of the patient’s occlusion causing disharmony such as an anterior open bite or apertognathia (Fig 7). Apertognathia develops in pipe smokers and usually occurs unilaterally on the smoker’s favorite side. Treatment would
Smoking and Staining, Abrasion, and Malocclusion Smoking may be one of several ways to acquire extrinsic or exogenous staining of the teeth. Tar and other by-products of combustion become deposits on the tooth surface, which usually appear as dark brown to black discoloration on the cervical aspect of the tooth45
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Figure 6.
Dental abrasion.
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Figure 7. Apertognathia secondary to pipe smoking. This patient had been a pipe smoker for many years.
generally consist of crown restorations of the occluding teeth.
Smoking and Alveolar Osteitis Alveolar osteitis or “dry socket” is a potential complication of tooth extraction, particularly of mandibular third molars.43,44 Although the etiology is still not fully understood, it has a prevalence from 2.6% to 11% in nonsmokers.42,43 This condition usually presents as a severe, throbbing pain in the alveolus of the surgical site for 2 or more days postoperatively.42 Denuded bone, odor, or a greyish exudate may be present at the site.42 Studies have shown a significant difference in the incidence of alveolar osteitis between smokers and nonsmokers, with nonsmokers having an incidence from two43 to four and a half times higher42 than that of nonsmokers. Treatment generally consists of daily packing of the alveolus with a eugenol dressing until symptoms disappear, as this condition is not responsive to systemic analgesics alone.42
Smoking and Dental Implants The use of endosseous dental implants for tooth replacement of edentulous areas has become a more widely used and predictable practice. The achievement of integration of the dental implant with the alveolar bone, or osseointegration, is the primary goal following placement of the implant. Failure rates of this process are generally under 10% in nonsmokers,46 but have been shown to be over seven times higher in smokers than in nonsmokers.47 Although the relationship of smoking to the adverse effects on osseointegration is poorly understood, smokers have been shown to have lower bone density than nonsmokers.48 This is a primary predisposing factor for implant failure. The benefits of smoking cessation for as little as 9 weeks during implant healing has been shown to be significant with respect to implant osseointegration.47 Smokers should be cautioned regarding higher failure rates when this type of treatment is planned.
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Figure 8. Snuff keratosis. Note the gingival recession, mucosal changes, and remnants of smokeless tobacco.
Smokeless Tobacco and the Oral Mucosa There are three forms of smokeless tobacco used in the United States: moist snuff, chewing tobacco, and dry snuff. Moist snuff is the most common form of smokeless tobacco used in the United States today. It is made with moist, finely ground tobacco. Snuff is tucked or “dipped” between the gingiva and the lip or cheek. A second form is chewing tobacco consisting of shredded tobacco, which is sold either loose, in a bar, or as a “plug.” Synonymous names are “wad,” “quid,” “twist,” or “chaw.” Often, a golfball sized amount is placed in the cheek and sucked or chewed. Dry snuff is inhaled powdered tobacco. Dry snuff is used infrequently in the United States. Smokeless tobacco is also used in other parts of the world. It is used commonly in many regions in Asia. Here, smokeless tobacco is consumed in the forms of “nass,” “naswar,” and “pan.” Each year, 10 million to 16 million Americans use smokeless tobacco, with annual sales exceeding a billion dollars.49 Its use is increasing among young people in this country. The CDC analyzed data from a 1995 Youth Risk Behavior Survey and found an increasing prevalence in smokeless tobacco use among high school students 18 years of age and younger.50
Adverse Effects of Smokeless Tobacco The 1994 Report of the Surgeon General concluded that use of smokeless tobacco “can cause gingival recession, periodontal destruction and cancer of the mouth.”51 An oral lesion uniquely characteristic to smokeless tobacco users is “snuff dipper’s patch,” also called “tobacco chewer’s lesion” and “snuff keratosis” (Fig 8). Snuff dipper’s patch occurs in areas corresponding to the intraoral placement of the smokeless tobacco. The National Health and Nutrition Examination Survey has classified this lesion into one of three degrees according to its progression or severity.52
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Degree 1 lesions present with normal color to pale white or gray. Slight superficial wrinkling of the mucosa exists but may disappear upon manually stretching this tissue. The oral mucosa does not appear thickened. A Degree 2 lesion has undergone a distinct whitish-gray or an occasionally red color change. Obvious wrinkles are seen but the mucosa is still not thickened. The color change remains upon stretching of the lesion. Degree 3 lesions possess thickened oral mucosa with deep furrows in the surface epithelium. The mucosa remains whitish-gray and may also have red areas. This lesion persists when stretched. Treatment consists of tobacco-use cessation upon which resolution of the mucosal alterations are likely. If regression to normal appearance does not begin within 14 days, biopsy and histological evaluation are warranted. Close follow-up is in order owing to the precancerous nature of these lesions.
Conclusions It has been well recognized that tobacco can induce changes in the gingiva, oral mucosa, and dentition. Careful history taking can identify smoking or tobacco use as a risk factor in patients with periodontal disease. Not only are these individuals more susceptible to periodontal disease, but smokers also have a poorer response to dental therapies. Thorough clinical examination can reveal the detrimental effects that tobacco has on the teeth and oral mucosa. Cessation of the habit may stop the progression of ill effects on the oral cavity. The adverse effects may be completely preventable in those who never use tobacco. Precancerous lesions merit special concern for both the health professional and the patient. Most benign lesions respond favorably to cessation of the habit. It is uncertain, though, which lesions will undergo dysplastic or malignant transformation. It is also important to note that not all cancerous conditions are preceded by benign lesions. For these reasons, tobacco use necessitates periodic, complete intraoral exams.
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