CHAPTER 14 Smoking and Periodontal Disease

M John Novak and Karen F. Novak

An estimated 27.9% of dentate U.S. adults are current smokers, and 23.3% are
former smokers. The prevalence of smoking is higher in individuals older than 34
years of age compared with with older age groups and in males (30.9%) compared
with females (25.1%), with the highest prevalence seen in non-Hispanic black men
(38.6%). Current smoking is more common among low-income adults (37.1%)
compared with medium- or high-income earners and increases with decreasing years
of education.
Increasing evidence points to smoking as a major risk factor for periodontitis,
affecting the prevalence, extent, and severity of disease. In addition, smoking may
influence the clinical outcome of nonsurgical and surgical therapy as well as the longterm success of implant placement. With 41.9% of periodontitis cases in the United
States associated with smoking, it has become increasingly important to understand
its impact on the initiation, progression, and management of the disease in patients
who smoke. This chapter discusses the effects of smoking on the prevalence, severity,
etiology, and pathogenesis of periodontal disease as well as the impact on treatment.
The reader is referred to several excellent reviews on the topic for the detailed results
of studies.

EFFECTS OF SMOKING ON PREVALENCE AND SEVERITY OF

PERIODONTAL DISEASE
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. In addition, crosssectional studies have consistently demonstrated that smokers present with less
gingival inflammation than nonsmoker. 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.
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.

TABLE 14-1 Effects of Smoking on Prevalence and Severity of Periodontal

Disease
Periodontal Disease
Impact of Smoking Gingivitis 'Gingival inflammation and bleeding on
probing Periodontitis /Prevalence and severity of periodontal destruction /Pocket
depth, attachment loss, and bone loss /Rate of periodontal destruction /Prevalence of
severe periodontitis /Tooth loss /Prevalence with increased number of cigarettes
smoked per day /Prevalence and severity with smoking cessation Decreased,
increased.
An assessment of the relationship between cigarette smoking and periodontitis
was performed in more than 12,000 dentate individuals over age 18 years as part of
the third National Health and Nutrition Examination Survey (NHANES
III).Periodontitis was defined as one or more sites with clinical attachment loss of 4
mm or greater and pocket depth of 4 mm or greater. Using criteria established by the
Centers for Disease Control and Prevention (CDC), "current smokers" were defined
as those who had smoked 100 or more cigarettes over their lifetime and smoked at the
time of the interview; "former smokers" had smoked 100 or more cigarettes in their
lifetime but were not currently smoking; and "nonsmokers" had not smoked 100 or
more cigarettes in their lifetime. Of the 12,000 individuals studied, 9.2% had
periodontitis. This represented approximately 15 million cases of periodontitis in the
United States. 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 1.68 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 was 2.79, 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
U.S. adult population were attributable to current smoking, and approximately 11%
(1.7 million cases) were attributable to former smoking.
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 - 50 from as low as 1.5 to as high as 7.3,
depending on the observed severity of periodontitis. A meta-analysis 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.42 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/I and the number of years of tobacco use is a
significant factor in tooth loss, coronal root caries, and periodontal disease.a Smoking
also has been shown to affect periodontal disease severity in younger individuals.
Cigarette smoking is associated with increased severity of generalized aggressive

periodontitis (formerly termed "early-onset periodontitis") in young adults and those

age 19 to 30 years who smoke are 3.8 times more likely to have periodontitis than
nonsmokers! Longitudinal studies have demonstrated thatzoung individuals smoking
more than 15 cigarettes per day showed the highest risk for tooth loss. Also, smokers
are more than six times as likely as nonsmokers to demonstrate continued attachment
loss. Over a 10-year period, bone loss has been reported to be twice as rapid in
smokers as in non-smokersli and proceeds more rapidly even in the presence of
excellent plaque control.
Less information is available on the effects of cigar and pipe smoking, but it
aTears that effects similar to cigarette smoking may be observed with these forms of
tobacco use. The prevalence of moderate and severe periodontitis and the percentage
of teeth with 5 mm or more of 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 a Tooth loss is also increased
in cigar and pipe smokers compared with nonsmokers. Smokeless tobacco use has
been associated with oral leukoplakia and carcinoma. However, no generalized
effects on periodontal disease progression seem to occur, other than localized
attachment loss and recession at the site of tobacco product placement.
Interestingly, former smokers have less risk for periodontitis than current
smokers but more risk than non-smokers, and the risk for periodontitis decreases with
the increasing number of years since quitting smoking. This suggests that (1) the
effects of smoking on the host are reversible with smoking cessation and (2) smoking

cessation programs should be an integral component of periodontal education and

therapy. Several tobacco intervention approaches can be used in helping the patient
deal with the nicotine withdrawal symptoms and psychologic factors associated with
smoking cessation. An appropriate approach for the dental office is the five-step
program recommended by the Agency for Health.

TABLE 14-2 Effects of Smoking on Etiology and Pathogenesis of Periodontal

Disease
Etiologic Factor Impact of Smoking Impact of Smoking Microbiology No
effect on rate of plaque accumulation /Colonization of shallow periodontal pockets by
periodontal pathogens /Levels of periodontal pathogens in deep periodontal pockets
Immunology Altered neutrophil chemotaxis, phagocytosis, and oxidative burst /TINF
a and PGE2 in gingival crevicular fluid (GCF) /1Ieutrophil collagenase and
elastase in GCF /Production of PGE2 by monocytes in response to LPS
Physiology ,Gingival blood vessels with j inflammation ,(GCF flow and bleeding on
probing with inflammation ISubgingival temperature /Time needed to recover from
local anesthesia /, Increased; decreased; TIVFNF tumor necrosis factor alpha, PGE,
prostaglandin E; LPS; lipopolysaccharide. Care Research and Quality.3A This
program uses the "five As" approach for smoking cessation: (1) ask (identify patient's
tobacco use status), (2) advise (on associations between oral disease and smoking and
the benefits of cessation), (3) assess (patient's interest and readiness to participate in
tobacco cessation programs), (4) assist (use appropriate techniques to assist patient in

tobacco cessation), and (5) range (follow-up contacts with the patiene In addition,
pharmacotherapeutic treatments such as nicotine replacement therapy and sustained
bupropion administration have proved effective.

EFFECTS OF SMOKING ON ETIOLOGY AND PATHOGENESIS OF

PERIODONTAL DISEASE
The increased prevalence and severity of periodontal destruction associated
with smoking suggests that the host-bacterial interactions normally seen in chronic
periodontitis are altered, resulting in more aggressive periodontal breakdown (Table
14-2). This imbalance between bacterial challenge and host response may be caused
by changes in the composition of the subgingival plaque, with increases in the
numbers and virulence of pathogenic organisms, changes in the host response to the
bacterial challenge, or a combination of both. This section discusses recent evidence
on the effects of smoking on the microbiology, immunology, and physiology of
periodontitis.

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). 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 Actinobacillus
actinomycetemcomitans, Porphyromonas gingivalis, and Prevotella intermedia. In a
similar study of 615 patients using immunoassay, the prevalence of A.
actinomycetemcomitans, P. gingivalis, P. intermedia, and Eikenella corroders was not
found to be significantly different between smokers and nonsmokers.
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 Bacteroides forsythus (now Tcmnerella
forsythia) and that smokers were 2.3 times more likely to harbor T forsythia than
nonsmokers and former smokers. 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.
Many discrepancies between the findings of micro-biologic 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.2 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.

Immunology
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 response from within the gingival tissues, with
no resulting loss of periodontal support. In contrast, periodontitis appears to be
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 immune

response, or a combination of both elements.
Smoking exerts a major effect on the protective elements of the immune
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 downregulation 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. In vitro studies of the effects of
tobacco products on neutrophils have shown detrimental effects on cell movement as
well as the oxidative burst. In addition, the production of antibody essential for
phagocytosis and killing of bacteria, specifically, immunoglobulin G2 (IgG2) levels
to periodontalpathogens, has been reported to be reduced in smokers versus
nonsmokers with periodontitis, suggesting suggesting that smokers may have reduced
protection against periodontal infection. In contrast, elevated levels of tumor necrosis
factor alpha (TNF-a) have been demonstrated in the gingival crevicular fluid (GCF)
of smokers, as well as elevated levels of prostaglandin E2 (PGE2), neutrophil

elastase, and matrix metalloproteinase-8 (IsAMP-8). In vitro studies also have shown
that exposure to nicotine increases the secretion of PGE2 by monocytes in response to
lipopolysaccharide (LPS).
These data suggest that smoking may impair the response of neutrophils to
periodontal infection 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 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. 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, the response of the microcirculation to plaque accumulation appears to
be altered in smokers compared with non-smokers. With developing inflammation,
increases in GCF flow, bleeding on probing, and gingival blood vessels were 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! Subgingival temperatures are

lower in smokers than nonsmokers, and recover from the vasoconstriction caused by
local anaesthetic administration takes longer in smokers.

SCIENCE TRANSFER
Smoking has detrimental effects on the periodontium, which can be observed
particularly in regard to periodontal therapy. Although the exact mechanisms are not
known, it appears that the host response to bacterial plaque and the ability of the
wound healing response in the host are significantly affected. Much of the
impairment centers on vascularity and the functions of vascularity, such as the ability
to provide oxygen, nutrients, cells, and growth stimulants to the tissues. Even slight
alteration in the vascularity can have significant and profound effects on tissues and
may account for the diminished response of periodontal therapy in smokers.
Importantly, cessation of smoking appears to allow the host to respond more like
nonsmokers, and therefore the effects on the vascularity appear reversible. This
provides the basis for smoking cessation therapies and attests to the resiliency of the
host.
A reduced gingival vascular response to dental plaque has been documented in
smokers compared with non-smokers. This is associated with an increased severity of
periodontal disease directly related to quantitative assessments of cigarette utilization.
Clinicians must be focused in their assessment of periodontal disease in smokers
because the appearance of healthy-appearing nonbleeding gingiva often is
accompanied by deep pockets and advanced bone loss. Cigarette smoking reduces the

favorable outcomes of periodontal therapy. This is most dramatic in mucogingival

root coverage surgical procedures and regenerative surgical procedures such as
guided tissue regeneration and bone grafts. It is recommended that smoking patients
should be following a successful smoking cessation program before these surgical
procedures are implemented.
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.

EFFECTS OF SMOKING ON RESPONSE TO PERIODONTAL THERAPY

Nonsurgical Therapy
Numerous studies have indicated that current smokers do not respond as well
to periodontal therapy as non-smokers or former smokers (Table 14-3). The majority
of clinical research supports the observation that pocket depth reduction is more
effective in nonsmokers than in smokers after nonsurgical periodontal therapy (Phase
I therapy), including oral hygiene instruction, scaling, and root planing.-

TABLE 14-3 Effects of Smoking on Response to Periodontal Therapy

Therapy Effects of Smoking Nonsurgical 'Clinical response to scaling and
root planing 'Reduction in pocket depth "Gain in clinical attachment levels 'Negative
impact of smoking with Ilevel of plaque control Surgery and implants "Pocket depth
reduction after surgery

+IDeterioration of furcations after surgery

"Gain in clinical attachment levels, I bone fill, recession, and T membrane
exposure after GTR
'Pocket depth reduction after DFDBA
'Pocket depth reduction and gain in clinical attachment levels after open flap
debridement
Conflicting data on the impact of smoking on implant success. Smoking
cessation should be recommended before implants. Maintenance Pocket depth during
maintenance therapy. Gain in clinical attachment levels Recurrent (refractory) disease
/Recurrent/refractory disease in smokers. Need for re-treatment in smokers.
Need for antibiotics in smokers to control the negative effects of periodontal
infection on surgical outcomes.
Tooth loss in smokers after surgical therapy

In addition, gains in clinical attachment as a result of scaling and root planing

are less pronounced in smokers than in nonsmokers. In a study of patients with
previously untreated advanced periodontal disease, scaling and root planing plus oral
hygiene resulted in significantly greater average reductions in pocket depth and
bleedinf on probing in nonsmokers than in smokers when evaluated 6 months after
completion of therapy. 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, even

though plaque scores were less than favorable. In another study, the nonsurgical
management of pockets 5 mm or greater showed that smokers had less pocket depth
reduction than nonsmokers after 3 months (1.29 vs. 1.76 mm) as well as fewer gains
in clinical attachment levels. 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 become clinically less significant. When pockets
persist in smokers and nonsmokers after therapy, adjunctive topical antimicrobial
therapy can be used to try to resolve the remaining pocket depths. When scaling and
root planing are used in combination with topical subgingivally placed tetracycline
fibers, subgingival minocycline gel, or subgingival metronidazole gel, smokers
continue to show less pocket reduction than nonsmokers.
It can be concluded that smokers respond less well to nonsurgical therapy than
nonsmokers. With excellent plaque control, however, these differences may be
minimised. When comparing current smokers with former smokers and nonsmokers,
the former and nonsmoking subjects appear to respond equally well to nonsurgical
care, reinforcing the need for patients to be informed of the benefits of smoking
cessation.

Surgical Therapy and Implants

The less favorable response of the periodontal tissues to nonsurgical therapy
that is observed in current smokers also appears to apply to 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
519 cigarettes/day) consistently showed less pocket reduction and less gain in clinical
attachment levels than nonsmokers or former smokers. These differences began
immediately after the completion of therapy and continued throughout 7 years of
supportive periodontal therapy. During the 7 years, deterioration of 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) and the treatment of intrabony defects by bone
allografts.By 12 months after GTR, therapy for deep intrabony defects, smokers
gained less than half as much clinical attachment as nonsmokers (2.1 vs. 5.2 mm). In
a second study, 73 smokers also showed less gain in clinical attachment (1.2 vs. 3.2
mm), more gingival recession, and less gain in bone fill of the defect. In addition, the
GTR membranes were exposed in all the smokers and approximately half the
nonsmokers (Table 14-4).

TABLE 14-4 Postsurgical Changes in Clinical Parameters of Healing Response

in Smoker and Nonsmoker Patients

Smokers Nonsmokers p Value CAL gain 1.2 1.3mm 3.2 2.0mm <0.007
GRincrease 2.8 1.2mm 1.3 1.3mm <0.008 PBL gain 0.5 1.5mm 3.7 2.2mm
<0.000

ME 10/10 15/28 c0.008

Modified from Trombelli M, Kim CK, Zimmerman GI, et al: J Clin Periodontol
24:366, 1997. CAL, Clinical attachment level; GR, gingival recession; PBL, probing
bone level; ME, prevalence of membrane exposure at removal.

Similarly, after the use of decalcified freeze-dried bone allograft (DFDBA) for
the treatment of intrabony defects, smokers showed less percentage of reduction in
presurgical pocket depth than nonsmokers (41.9% vs. 48.3%).
Open flap debridement surgery without regenerative or grafting procedures is
the most common surgical procedure used for accessing the root and osseous
surfaces. By 6 months after this procedure, smokers showed significantly less
reduction of deep pockets mm) than nonsmokers (3 mm for smokers vs. 4 mm for
nonsmokers) and significantly less gain in clinical attachment (1 8 vs. 2.8 mm), even
though the patients received supportive periodontal therapy every month for 6
months! Of increased significance 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 the
deep pockets in nonsmokers were 3 mm or less after completion of therapy.
The impact of smoking on implant success is unclear at present. Several
studies have shown that implant success rates are reduced in smokers, whereas other
studies have shown no effect. Since numerous factors can influence implant success
(see Chapters 7341) further controlled clinical trials are needed to address the role of
smoking as an independent variable in implant failure. However, with existing

evidence supporting a negative effect of smoking on long-term implant success,

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 effects of smoking on treatment outcomes appears to be longlasting 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 an
hygienist every 3 months for 7 years 36 Smokers consistently had deeper pockets
than nonsmokers and less gain in attachment when evaluated each year for the 7-year
period. Heavy smokers (20 cigarettes/day) had more plaque than light smokers,
former smokers, and nonsmokers. Even with more intensive maintenance therapy
given every month for 6 months after ap surgery, smokers had deeper and more
residual pockets than nonsmokers, even though no signicant differences in plaque or
bleeding on probing scores were found. These data suggest that the effects of
smoking on the quality of subgingival plaque, the host response, and the healing
characteristics of the periodontal tissues may have a long-term effect on pocket
resolution in smokers that may not be managed by conventional periodontal therapy.
More studies are needed to examine the effects of antimicrobial agents combined
with host-modulating agents in an attempt to control periodontal disease in smokers.

Recurrent (Refractory) Disease

Because of the difficulty in controlling periodontal disease in smokers, many
smokers become refractory to traditional periodontal treatment and tend to show more
periodontal breakdown than nonsmokers after therapy. The question has been raised
as to whether patients are truly refractive to therapy or whether the therapy
administered was insufficient to control the disease process. It is now thought that
patients formerly considered refractive to therapy actually undergo continuous or
recurrent disease; for this reason, the diagnosis of refractory periodontitis" has been
removed as a distinct classification.
The complex effects of smoking on the subgingival microora and host
response provide a model for studying new modalities of therapy for controlling
periodontitis. 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 refractory patients were
smokers. In one study the mean age of the refractory patients was 42 years, and 28 of
the 31 refractory patients were smokers. Of the 31 patients, 19% had been retreated
once surgically for pocket elimination, 10% had been re-treated twice surgically, and
the patients had received an average of four episodes of adjunctive antibiotics. During
the course of treatment, 36% of patients had lost an average of three teeth (range l10).
It is clear from these studies that smokers (1) may present with periodontal
disease at an early age, (2) may be difficult to treat with conventional therapy, and (3)

may continue to have progressive or recurrent periodontitis leading to tooth loss.

Further studies are needed to determine the level and type of therapy required to
provide long-term maintenance of periodontal health in individuals who choose to
continue smoking.