Gingivitis

Controlled clinical studies have demonstrated that in human models of experimental gingivitis, the development of inflammation in response to plaque accumulation is reduced in smokers compared with nonsmokers (Table 26-1).^14,15 In addition, cross-sectional studies have consistently demonstrated that smokers present with less gingival inflammation than nonsmokers.^16-20 These data suggest that smokers have a decreased expression of clinical inflammation in the presence of plaque accumulation compared with nonsmokers. The microbiologic, immunologic, and physiologic factors that might account for this observation are discussed in detail later.

TABLE 26-1 Effects of Smoking on Prevalence and Severity of Periodontal Disease

↓, Decreased; ↑, increased.

Periodontitis

Although gingival inflammation in smokers appears to be reduced in response to plaque accumulation compared with nonsmokers, an overwhelming body of data points to smoking as a major risk factor for increasing the prevalence and severity of periodontal destruction. Multiple cross-sectional and longitudinal studies have demonstrated that pocket depth, attachment loss, and alveolar bone loss are more prevalent and severe in patients who smoke compared with nonsmokers.^8,9,12,13 An assessment of the relationship between cigarette smoking and periodontitis was performed in more than 12,000 dentate individuals >18 years of age as part of the third National Health and Nutrition Examination Survey (NHANES III).² Periodontitis was defined as one or more sites with clinical attachment loss ≥4 mm and pocket depth ≥4 mm. Smoking status was defined using criteria established by the Centers for Disease Control and Prevention (CDC) (see Box 26-1). Of >12,000 individuals studied, 9.2% had periodontitis. This represented approximately 15 million cases of periodontitis in the US. On average, smokers were four times as likely to have periodontitis as persons who had never smoked after adjusting for age, gender, race/ethnicity, education, and income/poverty ratio. Former smokers were 1.7 times more likely to have periodontitis than persons who had never smoked. This study also demonstrated a dose-response relationship between cigarettes smoked per day and the odds of having periodontitis. In subjects smoking nine or fewer cigarettes per day, the odds for having periodontitis were 2.8, whereas subjects smoking 31 or more cigarettes per day were almost six times more likely to have periodontitis. With former smokers, the odds of having periodontitis declined with the number of years since quitting. These data indicated that approximately 42% of periodontitis cases (6.4 million cases) in the US adult population were attributable to current smoking and approximately 11% (1.7 million cases) were attributable to former smoking. These data highlight the serious threat to dental public health posed by cigarette smoking and raise questions about the best methods for managing periodontitis in patients who smoke (Box 26-2).

These data are consistent with the findings of other cross-sectional studies performed in the United States and Europe. The odds ratio for periodontitis in current smokers has been estimated to range from as low as 1.5 to as high as 7.3, depending on the observed severity of periodontitis.¹¹ A metaanalysis of data from six such studies involving 2361 subjects indicated that current smokers were almost three times more likely to have severe periodontitis than nonsmokers.¹⁰ The detrimental impact of long-term smoking on the periodontal and dentate status of older adults has been clearly demonstrated. Older adult smokers are approximately three times more likely to have severe periodontal disease,^21,22 and the number of years of tobacco use is a significant factor in tooth loss, coronal root caries, and periodontal disease.^23,24

Smoking also has been shown to affect periodontal disease severity in younger individuals. Cigarette smoking is associated with increased severity of generalized aggressive periodontitis in young adults,²⁵ and those age 19 to 30 years who smoke are 3.8 times more likely to have periodontitis than nonsmokers.²⁶ Longitudinal studies have demonstrated that young individuals smoking more than 15 cigarettes per day showed the highest risk for tooth loss.²⁷ Also, smokers are more than six times as likely as nonsmokers to demonstrate continued attachment loss.²⁸ Over a 10-year period, bone loss has been reported to be twice as rapid in smokers as in nonsmokers²⁹ and proceeds more rapidly even in the presence of excellent plaque control.³⁰ Less information is available on the effects of cigar and pipe smoking, but it appears that effects similar to cigarette smoking are observed with these forms of tobacco use.^31-34 The prevalence of moderate and severe periodontitis and the percentage of teeth with ≥5 mm attachment loss was most severe in current cigarette smokers, but cigar and pipe smokers showed a severity of disease intermediate between the current cigarette smokers and nonsmokers.³¹ Tooth loss is also increased in cigar and pipe smokers compared with nonsmokers.³⁴

Interestingly, former smokers have less risk for periodontitis than current smokers but more risk than nonsmokers, and the risk for periodontitis decreases with the increasing number of years since quitting smoking.² This suggests that the negative effects of smoking on the host are reversible with smoking cessation and therefore that smoking cessation programs must be an integral component of periodontal education and therapy (Box 26-3). Several tobacco intervention approaches can be used in helping the patient deal with the nicotine withdrawal symptoms and psychologic factors associated with smoking cessation (Box 26-4).^35,36

Microbiology

Studies have failed to demonstrate a difference in the rate of plaque accumulation of smokers compared with nonsmokers, suggesting that if an alteration in the microbial challenge in smokers exists, it results from a qualitative rather than quantitative alteration in the plaque.¹⁷ Several studies have explored the possible changes in subgingival plaque caused by smoking, with conflicting and inconclusive results. In a study of 142 patients with chronic periodontitis, plaque samples from deep pockets (≥6 mm) showed no differences in the counts of Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, and Prevotella intermedia.³⁷ In a similar study of 615 patients using immunoassay, the prevalence of A. actinomycetemcomitans, P. gingivalis, P. intermedia, and Eikenella corrodens was not found to be significantly different between smokers and nonsmokers.³⁸ In contrast, other studies have shown differences in the microbial composition of subgingival plaque between smokers and nonsmokers. In a study of 798 subjects with different smoking histories, it was found that smokers had significantly higher levels of Tannerella forsythia (previously called Bacteroides forsythus) and that smokers were 2.3 times more likely to harbor T. forsythia than nonsmokers and former smokers.³⁹ Of particular interest was the observation that smokers do not respond to mechanical therapy as well as nonsmokers; this is associated with increased levels of T. forsythia, A. actinomycetemcomitans, and P. gingivalis remaining in the pockets after therapy in the smoking group when compared with nonsmokers.^40-43

Many discrepancies between the findings of microbiologic studies are a function of the methodology involved, including bacterial counts versus proportions or prevalence of bacteria, number of sites sampled and the pocket depths selected, the sampling technique, the disease status of the subject, and the methods of bacterial enumeration and data analysis. In an attempt to overcome some of these problems, a recent study sampled subgingival plaque from all teeth with the exception of third molars in 272 adult subjects, including 50 current smokers, 98 past smokers, and 124 nonsmokers.⁴⁴ Using checkerboard DNA-DNA hybridization technology to screen for 29 different subgingival species, it was found that members of the orange and red complexes, including Eikenella nodatum, Fusobacterium nucleatum ss vincentii, P. intermedia, Peptostreptococcus micros, Prevotella nigrescens, T. forsythia, P. gingivalis, and Treponema denticola, were significantly more prevalent in current smokers than in nonsmokers and former smokers. The increased prevalence of these periodontal pathogens was caused by an increased colonization of shallow sites (pocket depth ≤4 mm), with no differences among smokers, former smokers, and nonsmokers in pockets 4 mm or greater. In addition, these pathogenic bacteria were more prevalent in the maxilla than the mandible. These data suggest that smokers have a greater extent of colonization by periodontal pathogens than nonsmokers or former smokers and that this colonization may lead to an increased prevalence of periodontal breakdown.

Immune-Inflammatory Responses

The immune response of the host to plaque accumulation is essentially protective. In periodontal health and gingivitis, a balance exists between the bacterial challenge of plaque and the immune-inflammatory responses in the gingival tissues, with no resulting loss of periodontal support. In contrast, periodontitis is associated with an alteration in the host-bacterial balance that may be initiated by changes in the bacterial composition of subgingival plaque, changes in the host responses, or a combination of both.

Smoking exerts a major effect on the protective elements of the immune-inflammatory response, resulting in an increase in the extent and severity of periodontal destruction. The deleterious effects of smoking appear to result in part from a down-regulation of the immune response to bacterial challenge. The neutrophil is an important component of the host response to bacterial infection, and alterations in neutrophil number or function may result in localized and systemic infections. Critical functions of neutrophils include chemotaxis (directed locomotion from the bloodstream to the site of infection), phagocytosis (internalization of foreign particles such as bacteria), and killing using oxidative and nonoxidative mechanisms. Neutrophils obtained from the peripheral blood, oral cavity, or saliva of smokers or exposed in vitro to whole tobacco smoke or nicotine have been shown to demonstrate functional alterations in chemotaxis, phagocytosis, and the oxidative burst.^45,46 In vitro studies of the effects of tobacco products on neutrophils have shown detrimental effects on cell movement, as well as the oxidative burst.^47-51 In addition, levels of antibody to periodontal pathogens essential for phagocytosis and killing of bacteria, specifically immunoglobulin G2 (IgG2), have been reported to be reduced in smokers versus nonsmokers with periodontitis,^42,52-54 suggesting that smokers may have reduced protection against periodontal infection. In contrast, elevated levels of tumor necrosis factor alpha (TNF-α) have been demonstrated in the gingival crevicular fluid (GCF) of smokers,⁵⁵ as well as elevated levels of prostaglandin E₂ (PGE₂), neutrophil elastase, and matrix metalloproteinase-8 (MMP-8).⁵⁶ In vitro studies also have shown that exposure to nicotine increases the secretion of PGE₂ by monocytes in response to lipopolysaccharide (LPS).⁵⁷

These data suggest that smoking may impair the response of neutrophils to plaque bacteria but may also increase the release of tissue-destructive enzymes. The exact changes in the immunologic mechanisms involved in the rapid tissue destruction seen in smokers are currently unclear. Further studies are needed to define the effects of tobacco use on the immune-inflammatory response and tissue destruction in periodontitis.

Physiology

Previous studies have shown that the clinical signs of inflammation are less pronounced in smokers than in nonsmokers.^15,18 This may result from alterations in the inflammatory response in smokers, as outlined previously, or from alterations in the vascular response of the gingival tissues. Although no significant differences in the vascular density of healthy gingiva have been observed between smokers and nonsmokers,⁵⁸ the response of the microcirculation to plaque accumulation appears to be altered in smokers compared with nonsmokers. With developing inflammation, increases in GCF flow, bleeding on probing,¹⁴ and gingival blood vessels⁵⁹ are less in smokers than nonsmokers. In addition, the oxygen concentration in healthy gingival tissues appears to be less in smokers than nonsmokers, although this condition is reversed in the presence of moderate inflammation.⁶⁰ Subgingival temperatures are lower in smokers than nonsmokers,⁶¹ and recovery from the vasoconstriction caused by local anaesthetic administration takes longer in smokers.^62,63 These cumulative data suggest that significant alterations are present in the gingival microvasculature of smokers compared with nonsmokers and that these changes lead to decreased blood flow and decreased clinical signs of inflammation. This explains the long observed phenomenon of a transient increase in gingival bleeding when a smoker quits.

Nonsurgical Therapy

Numerous studies have indicated that current smokers do not respond as well to periodontal therapy as nonsmokers or former smokers (Table 26-4). The majority of clinical research supports the observation that pocket depth reduction is more effective in nonsmokers than in smokers after nonsurgical periodontal therapy, including oral hygiene instruction, scaling, and root planing.^{40-43, 64-66} In addition, gains in clinical attachment as a result of nonsurgical treatment are less pronounced in smokers than in nonsmokers. In a study of patients with previously untreated advanced periodontal disease, nonsurgical therapy resulted in significantly greater mean reductions in pocket depth and bleeding on probing in nonsmokers than in smokers when evaluated 6 months after completion of therapy.⁴³ Average pocket reductions of 2.5 mm for nonsmokers and 1.9 mm for smokers were observed in pockets that averaged 7 mm before treatment. In another study, the nonsurgical management of pockets ≥5 mm showed that smokers had less pocket depth reduction than nonsmokers after 3 months (1.29 mm versus 1.76 mm), as well as less gain in clinical attachment levels.⁴⁰ When a higher level of plaque control can be achieved as part of nonsurgical care, the differences in the resolution of 4 mm to 6 mm pockets between nonsmokers and smokers became clinically less significant.⁶⁶ It can be concluded that smokers respond less well to nonsurgical therapy than nonsmokers. With excellent plaque control, however, these differences may be minimized (but the emphasis is on truly excellent plaque control). When comparing current smokers with former smokers and nonsmokers, the former and nonsmoking subjects appear to respond equally well to nonsurgical care,⁴⁰ reinforcing the need for patients to be informed of the benefits of smoking cessation.

TABLE 26-4 Effects of Smoking on Response to Periodontal Therapy

↓, Decreased; ↑ increased; GTR, guided tissue regeneration.

Surgical Therapy and Implants

The less favorable response of the periodontal tissues to nonsurgical therapy that is observed in current smokers is also observed after surgical therapy. In a longitudinal comparative study of the effects of four different treatment modalities, including coronal scaling, root planing, modified Widman flap surgery, and osseous resection surgery, smokers (“heavy” defined as ≥20 cigarettes/day; “light” defined as ≤19 cigarettes/day) consistently showed less pocket reduction and less gain in clinical attachment than nonsmokers or former smokers.⁶⁵ These differences were evident immediately after the completion of therapy and continued throughout 7 years of supportive periodontal therapy. During the 7 years, deterioration at furcation areas was greater in heavy and light smokers than in former smokers and nonsmokers. Smoking also has been shown to have a negative impact on the outcomes of guided tissue regeneration (GTR)^67,68 and the treatment of infrabony defects by bone grafts.⁶⁹ By 12 months after GTR therapy at deep infrabony defects, smokers demonstrated less than half the attachment gain as nonsmokers (2.1 mm versus 5.2 mm).⁶⁷ In a second study, 73 smokers also showed less attachment gain than nonsmokers (1.2 mm versus 3.2 mm), more gingival recession, and less bone infill of the defect. Similarly, after the use of bone grafts for the treatment of infrabony defects, smokers showed less reduction in pocket depths than nonsmokers.⁶⁹

Open flap access surgery without regenerative or grafting procedures is the most common surgical procedure used for accessing the root and bone surfaces. By 6 months after this procedure, smokers showed significantly less reduction of deep pockets (≥7 mm) than nonsmokers (3.0 mm for smokers versus 4.0 mm for nonsmokers) and significantly less gain in clinical attachment (1.8 versus 2.8 mm), even though all of the patients received supportive periodontal therapy every month for 6 months.⁷⁰ Of clinical relevance was the observation that only 16% of deep pockets in smokers returned to 3 mm or less at 6 months after surgery, whereas 47% of deep pockets in nonsmokers were 3 mm or less after completion of therapy.

Three metaanalyses have investigated the influence of smoking on the short- and long-term outcomes of implant therapy and have identified that smoking increases the risk of implant failure.^71-73 These studies used various definitions to define implant failure, including implant loss, implant bone loss, mobility, pain, and periimplantitis. Overall, the risk for implant failure in smokers appears to be approximately double the risk for failure in nonsmokers, and the risks appear to be higher in maxillary implants and when implants are placed in poor quality bone. Smoking has also been shown to be a risk factor for periimplantitis, with a majority of studies showing a significant increase in periimplant bone loss compared with nonsmokers.⁷⁴ Collectively, these data indicate that implant failure is more common in smokers than nonsmokers, but since numerous factors can influence implant success (see Part 7), further controlled clinical trials are needed to address the role of smoking as an independent variable in implant failure. However, given the current evidence, patients should be informed and advised of the benefits of smoking cessation and the potential risks of smoking for implant failure.

Maintenance Therapy

The detrimental effect of smoking on treatment outcomes appears to be long-lasting and independent of the frequency of maintenance therapy. After four different modalities of therapy, including scaling, scaling and root planing, modified Widman flap surgery, and osseous surgery, maintenance therapy was performed by a hygienist every 3 months for 7 years.⁶⁵ Smokers consistently had deeper pockets than nonsmokers and less gain in attachment when evaluated each year for the 7-year period. Even with more intensive maintenance therapy given every month for 6 months after flap surgery,⁷⁰ smokers had deeper and more residual pockets than nonsmokers, even though no significant differences in plaque or bleeding on probing scores were found. These data suggest that the effects of smoking on the host response and the healing characteristics of the periodontal tissues may have a long-term effect on pocket resolution in smokers, possibly requiring more intensive management in the maintenance phase. Smokers also tend to experience more periodontal breakdown than nonsmokers after therapy.^75,76 In studies of patients who failed to respond to conventional therapy, including different combinations of oral hygiene instruction, scaling and root planing, surgery, and antibiotics, approximately 90% of these poorly responding patients were smokers.^75,77

It is clear from these studies that smokers (1) may present with periodontal disease at an early age, (2) may be difficult to treat effectively with conventional therapeutic strategies, and (3) may continue to have progressive or recurrent periodontitis. For this reason, smoking cessation counseling must be a cornerstone of periodontal therapy in smokers.