Impact of Tobacco Use on Periodontal Status

Georgia K. Johnson, D.D.S., M.S.; Nancy A. Slach, R.D.H., B.S.

Abstract: This article reviews the effects of smoked and smokeless tobacco on periodontal status, including the impact of smoking
on periodontal therapy and potential mechanisms for the adverse effects of tobacco on the periodontium. Approximately half of
periodontitis cases have been attributed to either current or former smoking. Both cigar and cigarette smokers have significantly
greater loss of bone height than nonsmokers, and there is a trend for pipe smokers to have more bone loss than nonsmokers.
Unlike smokers, who experience widespread periodontal destruction, the most prevalent effects of smokeless tobacco are
localized to the site of placement, in the form of gingival recession and white mucosal lesions. Smoking has an adverse effect on
all forms of periodontal therapy, and up to 90 percent of refractory periodontitis patients are smokers. The pathogenesis of
smoking-related periodontal destruction has been attributed to alterations in the microflora and/or host response. Some data
indicates that smoking may increase levels of certain periodontal pathogens, but there is more evidence that smoking has a
negative effect on host response, such as neutrophil function and antibody production. An encouraging finding is that periodontal
disease progression slows in patients who quit smoking and that these individuals have a similar response to periodontal therapy
as nonsmokers. The facts presented in this paper will assist dental health professionals in treatment-planning decisions and
provide them with important information to share with patients who use tobacco products.
Dr. Johnson is Professor and Head, and Ms. Slach is Assistant in Instruction, both with the Department of Periodontics, Dows
Institute for Dental Research, The University of Iowa College of Dentistry. Direct correspondence and requests for reprints to Dr.
Georgia K. Johnson, The University of Iowa, College of Dentistry, Department of Periodontics, S450 DSB, Iowa City, Iowa
52242-1001; 319-335-7238 phone; 319-335-7239 fax; [email protected] e-mail.
Key words: periodontitis/etiology, tobacco/adverse effects, smoking/adverse effects, tobacco smokeless/adverse effects, tobacco
cessation

F
or many years, smoking has been linked to lung than former, or never, smokers.4 More recently, based
disease, cancer, cardiovascular disease, and on data from the NHANES III study, which included
poor pregnancy outcomes, such as miscarriage 12,329 subjects eighteen years and older, Tomar and
and low birth weight.1 Over the past two decades, it Asma5 concluded that approximately half of peri-
has also been recognized that smoking is associated odontitis cases were attributable to either current
with periodontal disease. As early as the 1940s, (41.9 percent) smoking or former (10.9 percent)
Pindborg2,3 noted that acute necrotizing ulcerative smoking. Current smokers were about four times as
gingivitis was associated with smoking in the Dan- likely as never smokers to have periodontitis, after
ish Royal Marines. However, for other forms of pe- adjusting for age, gender, race, education, and in-
riodontal disease, the prevailing opinion for many come. Former smokers were 1.68 times more likely
years was that if smokers did have more periodontal to have periodontitis.
disease, it was probably due to differences in levels The Erie County study, which included 1,426
of plaque and calculus. Beginning in the 1980s, nu- adults aged twenty-five to seventy-four years, found
merous epidemiological studies that have controlled an association between smoking and attachment loss
for confounding variables, such as age, plaque, cal- after correcting for confounding factors such as age,
culus, gender, and socioeconomic status, have pro- plaque and calculus, gender, income, education, and
vided strong evidence that smoking is a risk factor socioeconomic status.6 The odds for greater attach-
for periodontitis. ment loss in smokers as compared to nonsmokers
ranged from 2.05 in light smokers up to 4.75 in heavy
smokers. This study also examined the risk for bone
Smoking and Periodontitis loss in 1,361 of the study participants. The risk of
bone loss in smokers was even greater than that for
Results from the first United States National attachment loss, with smokers having odds ranging
Health and Nutrition Examination Survey (NHANES from 3.25 for light smokers to 7.28 for heavy smok-
I) demonstrated that, even though current smokers ers. A strong dose response was noted between smok-
had higher levels of plaque and calculus, after ad- ing and bone loss.7 Collectively, these epidemiologi-
justing for oral hygiene and other confounding vari- cal studies show that, after correcting for plaque and
ables, they still had greater periodontal destruction other confounding variables, smokers have at least

April 2001 ■ Journal of Dental Education 313

 three times the odds of having severe periodontitis
than nonsmokers.8 Response to Periodontal
Only a few prospective studies have evaluated
the longitudinal effects of smoking on periodontal Therapy in Smokers
health.9-15 The most recent of these investigated the
Several studies have found that up to 90 per-
effect of smoking exposure on periodontal status over
cent of refractory periodontitis patients are smok-
a ten-year period.13 That study found that the rate of
ers.38-40 In a six-year longitudinal study, most of the
bone loss in smokers was almost four times greater
patients with a high incidence of breakdown were
than that of nonsmokers.
smokers.41 Among maintenance patients who were
Many clinicians have noted a high prevalence
followed for five to eight years in a private periodontal
of smoking among young patients with aggressive
practice setting, patients who smoked were more than
periodontitis. Haber and coworkers estimated that as
twice as likely to lose teeth as nonsmokers.33 Collec-
much as 51 percent of periodontitis in nineteen- to
tively, these studies clearly demonstrate that smok-
thirty-year-olds is associated with smoking16; the
ing impairs the response to periodontal therapy.
prevalence of periodontitis was almost four times
A number of clinical studies have compared
higher in smokers than nonsmokers in that age
the response of smokers and nonsmokers to various
group.17 Other studies have also demonstrated that,
types of periodontal therapy, including nonsurgical
despite similar plaque levels, smokers in their twen-
and surgical therapy.42-53 Most of these studies show
ties and thirties have deeper probing depths and more
significantly less improvement in clinical parameters
attachment loss.18,19 The generalized form of aggres-
among smokers than nonsmokers. In a six-year lon-
sive periodontitis (formerly referred to as “general-
gitudinal study, smokers had approximately 50 per-
ized early-onset periodontitis”) is more associated
cent less improvement in probing depth and clinical
with smoking than the localized form of aggressive
attachment levels than nonsmokers.42
periodontitis (formerly referred to as “localized ju-
Smoking has a strong negative impact on re-
venile periodontitis”).20,21
generative therapy, including osseous grafting,54
In general, calculus deposits are also greater
guided tissue regeneration,55,56 or a combination of
in smokers,18,22,23 although amounts of plaque are vari-
these treatments.57 After correcting for plaque and
able.18,22,24,25 The effects of smoking on gingival in-
original defects, at one year smokers had significantly
flammation are equivocal,25-30 although the trend is
less attachment gain (2.1 + 1.2 mm) following guided
towards decreased inflammation. Smokers have a
tissue regeneration in infrabony defects as compared
higher prevalence of furcation involvement as as-
to nonsmokers (5.2 + 1.9 mm).58 Poor oral hygiene,
sessed by radiographic evidence of bone loss,31,32 and
smoking, and lack of recall compliance were associ-
clinical evaluation demonstrates both a higher preva-
ated with breakdown over a five-year period follow-
lence and severity of furcation attachment loss.32
ing guided tissue regeneration or scaling and root
Furthermore, smokers experience greater tooth loss
planing.59
than nonsmokers.32-36
The majority of studies show that gingival
As smokers have a higher prevalence and se-
grafting for root coverage is less successful in smok-
verity of periodontitis, it is not surprising that one
ers than nonsmokers.60-62 Some clinicians believe that
study reported that 75 percent of patients referred to
smoking is a relative contraindication to dental im-
a periodontist were either current or past smokers,
plant therapy. Early failures, before loading, in the
as compared to 54 percent of patients in general prac-
maxilla were higher in smokers (9 percent) than non-
tices.37 In fact, Haber and Kent37 reported that pa-
smokers (2 percent).63 Over an average of a thirty-
tients with moderate to advanced periodontitis who
eight-month follow-up, Bain and Moy64 reported that
were referred to a periodontal practice had 2.6 times
implant failure rates were more than twice as high in
the odds of a smoking history compared to patients
smokers (11.28 percent) as nonsmokers (4.76 per-
in the general practice who had no history of peri-
cent). Effects were most pronounced in the maxil-
odontitis.

314 Journal of Dental Education ■ Volume 65, No. 4

lary arch, where the failure rate for smokers was of smokeless tobacco are localized to the site of place-
16.82 percent in the anterior region as compared to ment. The primary periodontal alteration in smoke-
3.60 percent in nonsmokers. In a fifteen-year longi- less tobacco users is localized gingival recession. In
tudinal study of implants supporting mandibular general, gingival recession occurs in 25-30 percent
fixed prostheses, only 1 percent of implants were lost, of these users, and white mucosal lesions occur in
but smokers demonstrated significantly more bone 50-60 percent of users.71-73 The higher prevalence of
loss than former or never smokers.65 mucosal lesions as compared to gingival lesions is
probably due to the closer proximity of the tobacco
to the mucosal tissues.
Other Forms of Tobacco and Although the severity of white mucosal lesions
is related to the amount and duration of smokeless
Periodontal Status tobacco use,74 it is noteworthy that these alterations
are seen in teens that have used tobacco for short
In the United States, cigar consumption de- periods of two to three years. In one study, 56 per-
clined by 66 percent from 1964 until 1993. How- cent of smokeless tobacco users developed white le-
ever, between 1993 and 1997, overall cigar consump- sions within seven days of placement of smokeless
tion increased almost 50 percent.66 This increase has tobacco at a new site.75 Inflammatory mediators, such
been attributed to cigar smoking among young adults as prostaglandin E2 (PGE2) and interleukin–1 (IL-
who tend to smoke specialty cigars.67 Data from the 1) are elevated in these developing sites,75 and IL-1
Veterans Administration Dental Longitudinal Study,12 remains elevated in the established lesion.76 In the
which was begun in 1968, demonstrated that both developing lesion, the pro-inflammatory effects of
cigar and cigarette smokers had significantly more these mediators likely contribute to the observed
bone loss than nonsmokers (p<0.01), and there was erythema. In addition, both PGE2 and IL-1 influ-
a trend for pipe smokers to have even more bone ence keratinocyte proliferation,77,78 which has impli-
loss than nonsmokers (p=0.17). As compared to cations for development of the hyperplastic epithe-
nonsmokers, the relative risk of tooth loss in pipe lial lesion. Exposure of keratinocytes 79 and
and cigarette smokers was 1.6 as compared to 1.3 in monocytes80 to aqueous extracts of smokeless to-
cigar smokers. This study included 690 subjects, 50 bacco increases production of these mediators and
of whom were cigar smokers, 32 pipe smokers, 141 increases keratinocyte proliferation.81
cigarette smokers, and 477 nonsmokers. Therefore, The majority of the white mucosal lesions re-
the number of cigar and pipe smokers was relatively gress when the smokeless tobacco habit is discon-
small. tinued. Martin and coworkers82 reported that among
In 1991, 5.3 million (2.9 percent) of U.S. adults healthy, male Air Force basic trainees, 97 percent of
were current smokeless tobacco users. Regional dif- smokeless tobacco-induced lesions resolved within
ferences exist in usage, with smokeless tobacco use six weeks of tobacco cessation. In another study, 22
most popular in the southern United States and in percent of lesions resolved one week after tobacco
rural areas. Data from 1997 showed differences in exposure ceased.75 The clinician can use this infor-
prevalence of more than sixfold, from 1.4 percent in mation to guide decisions regarding the timing of
Arizona to 8.8 percent in West Virginia.68 In men the biopsies in smokeless tobacco users.
prevalence of use is greatest among young males aged
eighteen to twenty-four years and for women among
those aged over seventy-five years.69 However, these
figures do not include individuals under eighteen
Pathogenesis of Smoking-
years, and this is where the greatest increase in use Related Periodontal
has been seen. Advertising targets young males, as-
sociating smokeless tobacco use with virility, athlet- Destruction
ics, and the great outdoors. Approximately 16 per-
cent of high school male students report use of
smokeless tobacco in the past thirty days. Among Microbial Effects
young females use remains low at 1.5 percent.70
The increased prevalence and severity of peri-
Unlike cigarette smokers, who experience
odontitis in smokers cannot be explained by differ-
widespread periodontal destruction, the oral effects

April 2001 ■ Journal of Dental Education 315

 ences in the amount of plaque between smokers and chemotaxis,100 phagocytosis,38,101 and adherence.38 In
nonsmokers.6,13,18,24,35,83,84 Another possible explana- vitro nicotine or smoke treatment can inhibit pro-
tion is that smoking may alter the quality of the flora. duction of superoxide and hydrogen peroxide by
The oxygen tension in the periodontal pocket is lower stimulated neutrophils,102,103 which may inhibit mi-
in smokers, which may favor anaerobic species.85 crobial killing mechanisms and thus impair the host’s
Several studies indicate that the types of bacteria in ability to combat periodontal infection. On the other
smokers and nonsmokers did not vary significantly,86-89 hand, smoke exposure of unstimulated neutrophils
but data from the Erie County Study90 demonstrated has been shown to elevate the oxidative burst,103
that current smokers were 3.1 times more likely to which could enhance tissue destruction through di-
exhibit Actinobacillus actinomycetemcomitans infec- rect and indirect toxic effects. These various effects
tion and 2.3 times more likely to be infected with of smoking on neutrophil function may exacerbate
Bacteroides forsythus than former or never smok- smoking-related periodontal disease.
ers. In another study, smokers were eleven times more Antibody production is another protective host
likely to have a positive BANA reaction than non- mechanism that is altered by smoking. It is a fairly
smokers.91 A positive BANA reaction indicates the consistent finding that smoking decreases serum IgG
presence of Porphyromonas gingivalis, Trepenema concentrations.104,105 Serum IgG antibodies to certain
denticola, or B forsythus, which hydrolyze the trypsin periodontal pathogens have been reported to be re-
substrate.92 One explanation for these findings is that duced in smokers,16,106 and patients with aggressive
pathogens may be more difficult to eliminate in smok- periodontitis have decreased IgG2.107,108 One of the
ers. After scaling and root planing, fewer current mechanisms to explain this finding is that smoking
smokers were negative for P. gingivalis and B. decreases the proliferative capacity of T-cells, which
forsythus (p < 0.008), compared to never smokers affects B-cell function and antibody generation.93
and former smokers.45 Renvert and coworkers48 also Another factor to consider is that many of the
reported that A. actimomycetemcomitans was more tobacco components may be toxic to cells. In vitro
difficult to eliminate in smokers. nicotine treatment of root surfaces impairs fibroblast
attachment.109,110 Volatile components of cigarette
smoke (acrolein and acetaldehyde) have also been
Impact of Smoking on Host shown to inhibit gingival fibroblast attachment and
Response proliferation.111 Fibroblasts exposed to nicotine pro-
duce less fibronectin and collagen, whereas collage-
The primary etiology of periodontal disease is nase production was increased.112 These deleterious
bacteria; however, the host response determines a effects on fibroblast functions could impact wound
patient’s susceptibility to disease. There is strong healing and periodontitis progression.
evidence that smoking affects the innate and immune Smoking also has negative effects on bone
host responses.93 The findings of decreased inflam- metabolism. By the time they reach menopause,
mation26,27,94 and reduced gingival crevicular fluid women who smoke one pack of cigarettes a day
volumes in smokers as compared to nonsmokers95 throughout their adult lives will have an average defi-
suggest that smoking impairs gingival blood flow. cit in bone density of 5-8 percent.113 Recent reports
However, studies examining the effects of nicotine suggest that the combination of smoking and low
or smoking on gingival blood flow have shown con- systemic bone density negatively affects alveolar
flicting results.96 These varied results are likely re- bone height114 and density in postmenopausal fe-
lated to the dose of tobacco components, timing of males.115
measurements, and methodology employed to assess Smoking may influence osteoporosis and peri-
blood flow. Smoking impairs revascularization of odontitis by similar mechanisms. Of relevance to fe-
bone97 and soft tissues,98 which could have a major male smokers is that estrogen metabolism is altered
impact on wound healing, particularly as it relates to by smoking.116 Estrogen deficiency is associated with
regenerative and periodontal and implant therapies. elevations in IL-1, interleukin-6 (IL-6), and tumor
Neutrophils are the first line of defense against necrosis factor-alpha (TNF-alpha),117,118 which may
bacterial infection, and although smokers actually affect both alveolar and systemic bone status. To-
have significantly higher numbers of neutrophils in bacco components have also been shown to have di-
the peripheral circulation,99 their function is impaired. rect effects on certain bone resorptive mediators. The
Neutrophils from smokers have shown decreased

316 Journal of Dental Education ■ Volume 65, No. 4

combination of nicotine and bacterial lipopolysac-
charide (LPS) increased PGE2 secretion by periph- Summary
eral monocytes.119 Nicotine treatment increased IL-
6 production by cultured murine osteoblasts.120 In Tobacco users are at increased risk for oral dis-
human smokers, Tappia et al.121 reported that smok- ease. In smokeless tobacco users, the primary alter-
ers exposed to LPS had significantly higher plasma ations are white mucosal lesions and gingival reces-
levels of TNF alpha and IL-6 than nonsmokers. El- sion at the site of tobacco placement, which occur in
evated levels of TNF-alpha have been found in gin- 50-60 percent and 25-30 percent of smokeless to-
gival crevicular fluid (GCF) of smokers.122However, bacco users, respectively. Evidence supports smok-
no difference in GCF IL-1 beta or IL-1 receptor an- ing as a risk factor in chronic (adult) periodontitis
tagonist was identified between smokers and non- and periodontitis in young adults, as well as refrac-
smokers.123 Although nicotine increases IL-1 alpha tory periodontitis. Smokers are approximately three
and beta production by keratinocytes,124 it does not times more likely to have severe periodontitis than
affect IL-1 beta secretion by peripheral monocytes nonsmokers and exhibit about half as much improve-
or gingival mononuclear cells.119,125 In fact, the com- ment following periodontal therapy as nonsmokers.
bination of nicotine and LPS tends to downregulate Given the overwhelming evidence of the negative
IL-1 beta secretion.102,119 These findings indicate that impact of tobacco on periodontal status and the re-
different cell types respond differently to nicotine ex- sponse to periodontal therapy, the American Acad-
posure. Furthermore, while nicotine is the most emy of Periodontology’s Parameters of Care127 rec-
widely studied component of tobacco, tobacco prod- ommends tobacco cessation therapy for the
ucts contain thousands of chemicals that have the periodontal patient when appropriate. It is encour-
potential to influence host response, and additional aging to note that clinical studies demonstrate peri-
clinical studies are needed to clarify the effect of odontal disease progression slows in patients who
smoking on cytokine production. quit smoking and that these individuals have a simi-
lar response to periodontal therapy as nonsmokers.
These facts are important for treatment planning and
are powerful motivating factors for dental health pro-
Effects of Tobacco Cessation fessionals to use in tobacco cessation counseling.
on Periodontal Status
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