Smoking and periodontal

disease

CONTENTSIntroductionConstituents of tobacco smoke Mechanism of toxicityTobacco as a risk factorEffect of smoking on :

Plaque and oral floraPeriodontal tissuesImmunology

Smoking and systemic statusEffect of smoking on periodontal therapyTobacco cessationConclusionReferences

INTRODUCTION

INTRODUCTION Tobacco smoking - detrimental habit

In India Population

MalesFemales

- 1.1 billion

53%

47%

0.00%5.00%

10.00%15.00%20.00%25.00%30.00%35.00%

MalesFemales

Prevalence rate of smokers

NHFS 98-99

NHFS 05-06

25%29%

3.2% 2.8

%

Introduction

Deaths due to cancer

Other causesDue to smoking

Deaths due to habit

Series150 %

30 %

Death rate0%

10%20%30%40% 32%

6%

M F

Introduction

Different methods of tobacco smoking

Passive

Beedi

Cigars

Hookahs

Pipes

Cigarettes

Introduction

Heavy smokers> 20 / day

Former smokersQuit within the last 10 years

Light smokers< 20 / day

Risk factor for systemic diseases

Susceptibility to coronary artery disease: 2-4 times

Introduction

Introduction

Smoking and periodontal disease

Long-term chronic exposure

in prevalence and progression

Passive smoking – 30% of disease susceptibility

Introduction

Tobacco

smoking

Plaque and oral

flora

Periodontal

tissuesHomeostasis and

healing potentia

l

Systemic health

Immune respons

e

CONSTITUENTS OF TOBACCO SMOKE

CONSTITUENTS OF TOBACCO SMOKE

Complex mixture of substances – over 4000 known constituents

Phenols and cyanides – antibacterial and toxic properties

Constituents

Gaseous phase and particulate phase

Tar and nicotine yields reduced due to use of filters

Dose of tobacco intake – depends on the way an individual smokes

Constituents

Biochemical analyses of cotinine (Wall et al 1988)

Measurements are more reliable – longer half life of 14-20 hours (Jarvis et al 1988)

Cotinine concentrations of regular smokers

Resting plasma nicotine levels : 5–50 ng/ml

Plasma and salivary levels

~ 300 ng/ml (14 ng/ml – 1000

ng/ml)

Urine concentrations ~ 1500 ng/ml

Constituents

Absorption of nicotine Rapidly absorbed into blood - 30% in free

form Lipid-soluble Inhalation of tobacco smoke

Constituents

Action on organs blood pressure heart rate respiratory rate skin temperature Vasodilatation at other body sites

Constituents

Oral mucosa Slowly

From cigarette smoke pH 5.5 not well absorbed

From cigar and pipe smoke pH 8.5 good absorption

(Benowitz 1988)

MECHANISMS OF TOXICITY

MECHANISMS OF TOXICITY

Vascular alteration

antibody production(IgG2P7)

Immunosuppressive effect

Physical subgingival environment

Nicotine on root surfaces

bacterial adhesion to epithelial cells

Mechanisms of toxicity

Impaired immune response

Anaerobic subgingiv

al infection

Connective tissue

cytotoxicity

Impaired wound healing

in severity

of periodontal disease

TOBACCO AS A RISK FACTOR

TOBACCO AS A RISK FACTOR Based on Hill’s criteria (1965) for causation,

reviewed by Gelskey (1999)

Biologic plausibility

Strength of association

Consistency Specificity

Temporality Biologic gradient

Analogy

EFFECT OF SMOKING ON PLAQUE

Plaque developmentOral floraSubgingival microfloraCalculus formationConclusion

EFFECT OF SMOKING ON PLAQUE

Effect of smoking on plaque development

Higher prevalence of dental plaque in smokers(Kristoffersen 1970, Preber et al 1980)

In contrast, smoking did not appear to increase the amount of plaque (Alexander 1970, Sheiham 1971)

Experimental gingivitis models – rate of plaque formation was similar (Bastiaan & Waite 1978, Bergstrom 1981)

Effect of smoking on plaque

Effect of smoking on the oral flora

No significant trend for smokers to harbor putative pathogens (Mager et al 2003, Lie et al 1998b)

Increased counts of exogenous flora – E. coli and C. albicans – have been reported in smokers

Effect of smoking on plaque

Effect of smoking on the subgingival microflora

Cross-sectional investigations

No influence of smoking on the occurrence of any species

Zambon et al 1996 - higher prevalence of A. actinomycetemcomitans, T. forsythensis and P. gingivalisRisk of infection with T. forsythensis – 2.3 times

Mager 2003 – A. actinomycetemcomitans

Effect of smoking on plaque

Prevalence of B. forsythus and P. nigrescens maxilla > mandible (Haffajee

2001)

Cigarette smoking lowers redox potential increase in anaerobic bacteria

Eggert 2001 – effects of CO

Enhancing growth of anaerobes

Formation of advanced

glycation end products by

smoke

Effect of smoking on plaque

Effect of smoking on calculus formation

More supragingival calculus deposits (Bergstrom 1999)

Significantly more with pipe smokers than cigarette

Reason: salivary flow rates

calcium concentration, organic components

Effect of smoking on plaque

Conclusions

Numerous species in oral cavity Varied sampling methods Common known species often investigated

Trend: Greater numbers of pathogens not correlating with plaque levels

EFFECT OF SMOKING ON PERIODONTAL TISSUES

GingivaGingival blood flow Gingival vasculature Gingival inflammation and bleedingOxygen tension in gingival tissueGingival and PDL fibroblastsPeriodontitisWound healingConclusion

EFFECT OF SMOKING ON PERIODONTAL TISSUES

Effect of smoking on gingiva

Changes in the epithelium - hyperkeratotic, hyperplastic

Greyish discoloration of the gingiva

Increased amounts of IL-1, IL-6 and PGE2 (Johnson et al 1996)

Effect of smoking on periodontal tissues

Smoking – predisposing factor for ANUG

use of tobacco frequency of ANUG (Rowland 1999)

Reason: Tar in the smoke irritating effect on gingivaNicotine vasoconstriction of capillaries (Lindeboom 2005) 

Effect of smoking on periodontal tissues

Effect of smoking on gingival blood flow

Infusion of nicotine

• gingival blood flow• Recovery below

baseline levels

Transient decrease

(Clarke et al 1981)

Laser Doppler Flow study

• Gingival blood flow ~25%

• Maintained for 5 min• Gradually declined

to baseline values

Transient increase

(Baab & Oberg 1987)

Effect of smoking on periodontal tissues

Reason:Nicotine Vasoconstrictive property

In some cases, smoking-induced elevation in blood pressure overcomes vasoconstrictive effect of smoking.

Smoking decreases gingival blood flow

Effect of smoking on periodontal tissues

Bergstrom et al 1983

Nicotine

Sympathetic ganglia catecholaminesα - receptors

vasoconstrictionPeripheral blood vessels –

periodontium gingival bleeding

Vasoconstriction

Keratinization

Effect of smoking on periodontal tissues

Morozumi et al 2004 - following quitting At 3 days – significant increaseAt 4-8 weeks - small increases occurred

Effect of smoking on periodontal tissues

Effect on the gingival vasculature

number of vessels endothelial ICAM-1 expression

(Rezavandi et al 2002)

not accompanied by an equivalent increase in vascularityInflammation

-

Effect of smoking on periodontal tissues

Gingival inflammation and bleeding

Smokers experienced less gingival bleeding (Bergstrom & Floderus- Myrhed 1983)

NHANES III : Dose–response effect (Dietrich et al 2004)

Quit-smoking program – improvement in parameters(Nair et al 2003) Rapid recovery of the inflammatory response

Effect of smoking on periodontal tissues

gingival redness

Fewer gingival vessels

GCF

Less bleeding

sites

Suppression of the normal inflammatory

response

(Bergstrom 1986)

Effect of smoking on periodontal tissues

Oxygen tension in the gingival tissues

Carbon monoxide – reduces O2 tension (Scott et al 2001)

Oxygen saturation of haemoglobin – lower in healthy gingiva, higher with inflammation (Hanioka et al 2000b)

Pocket oxygen tensionSmokers Non-smokers

~ 21.9 mm Hg ~ 33.4 mm Hg

Effect of smoking on periodontal tissues

Effect on fibroblasts

Nicotine affects Production of collagenous, non-

collagenous proteins (Giannopoulou 2001) Cell orientation and attachment (Raulin et al

1988)

Effect on human gingival fibroblasts

Nicotine HGF

(Wendell 2001)

IL-6

IL-8

P. gingivalis

Effect of smoking on periodontal tissues

25–100 ng/ml of nicotine Orientation of cells lost (Tanur et al 2000)

10–75 g/ml of nicotine Inhibition of proliferation of gingival

fibroblasts production of type 1 collagen and

fibronectin collagenase activity in the culture media Cytoplasmic vacuolation Attachment disrupted (Tipton and Dabbous

1995)

Effect of smoking on periodontal tissues

Effect of acrolein and acetaldehyde Inhibited cell attachment and cell

proliferation (Cattaneo et al 2000, Poggi et al 2002)

EM changes:o Disruption of cell orientation o Presence of large vacuoles and residual

bodies o Reduction in cell viability o Disruption of the cytoskeletal structures

Effect of smoking on periodontal tissues

Root surface of tooth Alters fibroblast attachment Integrin expression Decrease collagen production Increase collagenase production

Nicotine levels could be reduced following root planing (Cuff et al 1989)

Effect of smoking on periodontal tissues

Effect on PDL fibroblasts

Dose-dependent inhibition

< 10 g/ml – no significant effect 100 ng/ml-2 g/ml – inhibition of

proliferation > 1mg/ml – vacuolation

(Giannopoulou et al 1999)

High concentrations (5–25mM) - cytotoxicity (Chang et al 2002)

Effect of smoking on periodontal tissues

Periodontitis

Relative risk for smokers : 3.97 former smokers : 1.68

Odds ratio – 1.5-7.3

Cigar and pipe smokers - severity of disease intermediate between current cigarette smokers and nonsmokers

Effect of smoking on periodontal tissues

Deeper probing depths and a larger number of deep pockets (Feldman et al 1983, Bergstrom et al 2000a)

Twin study - greater degree of alveolar bone loss and tooth loss in smokers (Bergstrom in 1983)

More attachment loss including more gingival recession (Grossi et al 1994, Haffajee & Socransky 2001a)

More teeth with furcation involvement (Mullally & Linden 1996)

Effect of smoking on periodontal tissues

Wound healing

Initial short-term healing after therapy (up to 6 weeks) Reduced cell function Reduced host defense response Reduced vascularity

Medium to longer term healing (3 months - 1 year) Cellular and tissue differences

Effect of smoking on periodontal tissues

Poorly functioning fibroblasts gingival tissue adaptation impaired

Poor healing

Persistence of infection

Predisposition to disease

Effect of smoking on periodontal tissues

Conclusions

Long-term chronic effect

Impairing the vasculature and revascularization

Following abstinence, the vasculature does return to a near- normal state

Smoking and periodontal

disease

CONTENTSIntroductionConstituents of tobacco smoke Mechanism of toxicityTobacco as a risk factorEffect of smoking on :

Plaque and oral floraPeriodontal tissuesImmunology

Smoking and systemic statusEffect of smoking on periodontal therapyTobacco cessationConclusionReferences

EFFECT OF SMOKING ON IMMUNOLOGY AND HOST

RESPONSEPMN functionLymphocyte functionGCFCytokinesOther factorsConclusion

EFFECT OF SMOKING ON IMMUNOLOGY AND HOST

RESPONSEEffect on PMN function

Systemic neutrophilia No effect on oral and sulcular neutrophils Reduction in numbers (Eichel & Shahrik 1969,

Pauletto et al 2000)

Effect of smoking on immunology and host response

Express several receptors

Metabolites of Endogenous smoke factors

34 subtype of nicotinic receptors

(Benhammou et al 2000)

IL-8, ICAM-1, TNF-

Effect of smoking on immunology and host response

PMN functi

on

Degradative

protease formation

Neutrophil respirator

y burst

PMN migration

and chemotaxi

s

Neutrophil priming

Effect of smoking on immunology and host response

Degradative protease formation from PMN

elastase activity and MMP-8 activity – refractory periodontitis (Soder B 1999)

Lower elastase concentrations in GCF PMNs are less functional (Wolff et al 1994) or are present in reduced quantities

Effect of smoking on immunology and host response

Neutrophil respiratory burst “Respiratory burst” – O2-dependent

phagocytosis

Cigarette smoke constituents may inhibit the respiratory burst (Drost et al 1992, Sorensen et al 2004)

Nicotine IL-8 ROS, particularly ONOO- (Iho et al 2003)

Metallothionein – protective roleResponses – enhanced or

suppressed ?

Effect of smoking on immunology and host response

Neutrophil migration and chemotaxis

Tobacco smoke exposure may impair f-actin kinetics

Hampers neutrophil motility and migration(Ryder et al

2002)

Neutrophil migration expression of adhesion integrins expression of selectins

Effect of smoking on immunology and host response

Neutrophil chemotaxis and phagocytosis (Seow et al 1994)

Dose-dependent suppression o Low concentrations – stimulatory to fMLP o High concentrations - inhibitory

Neutrophils respond to multiple chemotactic

stimuli

Results depend upon the experimental

system used

Effect of smoking on immunology and host response

Neutrophil priming (hyper-reactivity) Koethe et al 2000, Matheson et al 2003

Cigarette smoke condensate (CSC)

2-fold increase in fMLP-receptor expression

Subsequent stimulation with fMLP

Cells ‘‘primed’’

2-fold increase in superoxide and elastase release

Hyperinflammatory response

Effect of smoking on immunology and host response

Neutrophil priming capabilities for TNF-alpha (Gustafsson 2000, Bostrom et al 1998b)

HEALTH DISEASE

Effect of smoking on immunology and host response

Conclusions

Neutrophils - critical role

Effect of smoking on immunology and host response

Smoking And Lymphocyte Function

Immune system recognize antigens response

Lymphocytes

T lymphocyte

sNK cells

B lymphocyte

s

Effect of smoking on immunology and host response

T lymphocytes

Leucocytosis (Corre et al 1971, Hughes et al 1985)

Loos et al 2004 Non-smokers, light smokers or heavy

smokers Total leucocyte count - highest in heavy

smokers Increased neutrophil numbers

Effect of smoking on immunology and host response

Animal studies - chronic exposure of rats Vapour phase – no significant changes Particulate phase - confers

immunosuppressive properties

Nicotine, Benzo(a)pyrene,

Benzo(a)anthracene

Immunosuppressive

(Geng et al 1995, 1996)

Tobacco glycoprotein, Metals

Immunostimulatory

(Francus 1988, Brooks 1990)

Net effect - dependent upon dose and

duration

Effect of smoking on immunology and host response

T cell function – controversial

Reduction in proliferative response of lymphocytes to mitogens (Chang et al 1990, Johnson et al 1990)

No significant differences between control subjects, periodontitis patients and smoking status (Loos et al 2004)

Effect of smoking on immunology and host response

B cells and Immunoglobulins

B cells + Cytokines Plasma cells (Th-derived)

Chronic exposure to nicotine Impairment of antigen-mediated T cell signalling Inhibits antibody-forming cell responses

Immunosuppression(Sopori et al 1998)

Effect of smoking on immunology and host response

sIgG levels are reduced in smokers – IgG2 (Fredriksson 1999)

Effects of cigarette smoking on serum IgA and IgM classes – controversial

Smoking decreases salivary IgA

IgE is greatly elevated in smokers

Reduced antibody levels to periopathogens

Effect of smoking on immunology and host response

B cell function Decrease in proliferative response to B cell

mitogens and antigens (Sopori et al 1989) Smoking cessation, function returns to

normal (Reynolds et al 1991)

Combustion by-products - B cell function Tobacco glycoprotein - potent B cell

mitogenNet effect – depends on properties of

tobacco

Effect of smoking on immunology and host response

Natural killer (NK) cells

Antibody-dependent cellular cytotoxicity Analogous to cytotoxic T cells Produce chemokines and cytokines

Reduced activity in smokers (Tollerud et al 1989)

Reversible on smoking cessation (Meliska et al 1995)

Effect of smoking on immunology and host response

Conclusions

Inconsistencies and variations in findings

Inadequate knowledge of antigens and responses

Effect of smoking on immunology and host response

Gingival Crevicular Fluid GCF nicotine concentrations - 300 times that

of plasma (20ng/ml)

Lower resting GCF flow rate (Persson et al 1999)

Reduced GCF flow Defense mechanism hampered

Less flushing – removal of microbes and waste products

Effect of smoking on immunology and host response

Episode of smoking transient increase in GCF flow rate (McLaughlin et al 1993)

Quit-smoking programme – flow rate greater at 5 days postquitting (Morozumi et al 2004)

Effect of smoking on immunology and host response

Cytokines

Cytokine overproduction detrimental host response disease

Higher levels of TNF- (Bostrom et al 1998)

Dose-dependent effect of smoking on IL-1, IL-8, and MCP-1 levels (Kuschner et al 1996)

Effect of smoking on immunology and host response

Higher levels of IL-8, lower levels of IL-4 (Giannopoulou et al 2003)

IL-1 levels half of that found in non-smokers (Petropoulos et al 2004)

IL-6, IL-1 - no significant differences (Bostrom et al 2000)

Effect of smoking on immunology and host response

TGF- IGFIFN

IL-1, -6, -8TNF-

PG

The balance between protection and destruction is

mediated largely by the type of cytokine pattern

secreted by these cells.

Effect of smoking on immunology and host response

Other Factors

2-macroglobulin and 1-anti-trypsin levels Lower concentrations in heavy smokers

(Persson 2001)

ICAM-1 levels (Fraser et al 2001)

Smokers Non-smokers

Serum 331 ng/ml 238 ng/mlGCF 83 ng/ml 212 ng/ml

Effect of smoking on immunology and host response

Conclusions Logic – factors associated with tissue

destruction should be higher

However, lower levels with most cytokines

Clinically, low levels of inflammation observed

May indicate higher levels of activity

GCF could be an end product of the destructive

process

SMOKING AND SYSTEMIC STATUS

SMOKING AND SYSTEMIC STATUS

Smoking + systemic factors = risk of disease

Erie County study In diabetics, more periodontal attachment loss Odds ratio for attachment loss - 30 times more

o Diabetes and heavy smoking o > 45 years of ageo P. gingivalis or T. forsythensis

Postmenopausal women AIDS / HIV +ve

Smoking and systemic status

Gene polymorphisms

IL-1 genotype & smokers

(McGuire & Nunn, 1999)

bleeding on probing (Lang 2000)

probing depth and attachment loss

Risk factor Risk of tooth loss

IL-1 positive genotype 2.7Smoking 2.9 IL-1 positive + smoking 7.7

Smoking and systemic status

N-acetyltransferase 2 (NAT2)

Tobacco smoke Arylamines Detoxification Immunosuppressant

Polymorphism rapid or slow acetylators

Severe periodontal conditions – slow acetylators

NAT2 genotype-positive bone loss (Kocher 2002)

NAT2

Smoking and systemic status

Cytochrome P450 and glutathione S-transferase enzymes

Neutralization of toxic substances

Polymorphism risk of periodontitis

EFFECT OF SMOKING ON PERIODONTAL THERAPY

Non-surgical therapyAntimicrobial therapySurgical therapyTissue graftsImplant therapy Maintenance therapyRecurrent/refractory disease

EFFECT OF SMOKING ON PERIODONTAL THERAPY

Non-surgical therapy

Non-surgical therapy is less effective in smokers and non-smokers

Less reduction in probing depth Smaller levels of gain in clinical attachment

Effect of smoking on periodontal therapy

Grossi et al 1996 – 3-month study Pocket depth reduction - 1.29 vs 1.76 mm

Good plaque control – differences are less significant

Smokers respond less well to nonsurgical therapy

Effect of smoking on periodontal therapy

Antimicrobial therapy

Antimicrobial therapy as an adjunct

Widely used host modulators - tetracycline antibiotics Anti-inflammatory Anti-collagenase activity Anti-oxidant

Enhanced results with: Locally delivered minocycline microspheres

Effect of smoking on periodontal therapy

Little effect of systemic metronidazole (Soder et al)

Systemic amoxicillin and metronidazole – better results

Effect of smoking on periodontal therapy

Surgical therapy

Smokers treated with surgical periodontal therapy Less probing depth reduction Smaller gains in CAL Less gain in bone height

Kaldahl 1996 – 7-year follow up Deterioration of furcation areas

Level of recession - worse in smokers (Martinez-Canut et al 1995, Gunsolley et al 1998)

Effect of smoking on periodontal therapy

Tissue grafts Heavy cigarette smoking decreases the

amount of root coverage

Harris’ study (n=100) CT with partial thickness pedicle graft Light smokers - 97%

Heavy smokers- 99%Non-smokers - 98%

CT graft - more resistant to effects of smoking

Effect of smoking on periodontal therapy

Smoking - negative impact on outcomes of GTR, DFDBA

GTR with ePTFE membrane Smokers - 57% Non-smokers - 78%

Trombelli et al 1997

Effect of smoking on periodontal therapy

Implant therapy

Bain 1993 – 6-year follow-up studySuccess rate - > 95% (non-smokers)

< 89% (smokers)

Implant failure is 2.5 times greater (Wilson 1999)

Smoking cessation - 1/3rd as many failures as compared to smokers

Effect of smoking on periodontal therapy

Light smoking - no effect on machined or dual acid-etched surface implants (Bain 2002)

Maxillary implants risk for peri-implantitis Failures – twice more

Lindquist et al 1996 - 15-year longitudinal study Greater marginal bone loss around

mandibular implants

Effect of smoking on periodontal therapy

Maintenance therapy

2 times the risk of losing teeth

Scabbia 2001 - more residual pockets

Effects of smoking on treatment outcomes - long lasting

Effect of smoking on periodontal therapy

Recurrent/refractory disease

Smokers do not respond favorably recurrent or continuing disease

MacFarlane et al 1992 – 90% of subjects who showed poor results were smokers

Effect of smoking on periodontal therapy

Conclusion

Smoking detrimental effect on periodontal therapy

TOBACCO CESSATIONIntervention models for dental practice

1.Brief2.Comprehensive3.Pharmacotherapy

Relapse preventionEffect of cessation on PDL status and treatment

outcomes

TOBACCO CESSATION

Tobacco is harmful to health

Success long-term abstinence 6 months

Tobacco Cessation

Brief Intervention Program Agency for Health Care Research and Quality

(Fiore MC et al 2000)

Brief Interventi

on Program

ASK

ADVISE

ASSESS ASSIST

ARRANGE

Tobacco Cessation

Comprehensive Intervention Program

Expanding the scope of intervention

Expanding the five A’s1. Ask2. Advise3. Assess4. Assist (2-14% effectiveness)5. Arrange

Tobacco Cessation

Pharmacotherapy Nicotine replacement therapies

Others Sustained-release bupropion Clonidine, nortriptyline

OTC products

Nicotine chewing gum

Lozenges Patches

On prescriptions

Nasal sprays

Inhalers

Tobacco Cessation

Tobacco Cessation

Indications

Patient’s health history Current nicotine exposure Past experience with cessation

Tobacco Cessation

Nicotine replacement and combinations

< 20 / day – patch – 7–22 mg for 4 weeks or longer> 20 / day – combination; patch + other products

No use of any other form of tobacco when on a cessation program

Bupropion – 1st 3 days : 150 mg OD upto 7-12 weeks : BID Safe upto 6 months

Tobacco Cessation

Relapse prevention

Withdrawal symptoms after tobacco cessation

Relapse – high

Long-term abstinence

Alternate treatment modalities

Tobacco Cessation

Effect of cessation on PDL status and treatment outcomes

Rate of bone and attachment loss slows

Disease severity – intermediate

Former smokers respond to therapy similar to never smokers (Kaldahl et al 1996)

Bain 2002 - implant failures

CONCLUSIONAs an environmental factor, smoking

interacts with the host and the bacterial challenge, resulting in an increased susceptibility to periodontitis and poorer response to treatment.

Recent guidance suggest that dental practices should assess the smoking status of patients and motivate smokers towards quitting.

REFERENCES Jan Lindhe, Niklaus P. Lang, Thorkild Karring. 5th

Edition. Clinical Periodontology and Implant Dentistry. Blackwell Munksgaard 2008.

Rose LE, Genco RJ, Cohen DW, Mealy BL. Periodontal Medicine. B.C. Decker Inc 2000.

Palmer RM, Wilson RF, Hasan AS, Scott DA. Mechanisms of action of environmental factors – tobacco smoking. J Clin Peridontol 2005; 32 (Suppl. 6): 180–195.

Ana Pejčić, Radmila Obradović, Ljiljana Kesić, Draginja Kojović. Smoking and periodontal disease a review. Medicine and Biology Vol.14, No 2, 2007, pp. 53–59.

References

Georgia K. Johnson, Margaret Hill. Cigarette smoking and the periodontal patient. J Periodontol 2004; 75: 196–209.

Francisco Rivera-Hidalgo. Smoking and periodontal disease. Periodontology 2000, Vol. 32, 2003, 50–58.

D.F. Kinane and I.G. Chestnutt. Smoking and Periodontal Disease. CROBM 2000 11: 356.

Newman MG, Takei HH, Klokkevold PR, Carranza FA. Carranza’s Clinical Periodontology. 10th Edition. Saunders Elsevier 2007.

References

Mark I. Ryder. The influence of smoking on host responses in periodontal infections. Periodontology 2000, Vol. 43, 2007, 267–277.

Boström L, Bergström J, Dahle´n G, Linder LE. Smoking and subgingival microflora in periodontal disease. J Clin Periodontol 2001; 28: 212–219.

Antonella Labriola, Ian Needleman & David R. Moles. Systematic review of the effect of smoking on nonsurgical periodontal therapy. Periodontology 2000, Vol. 37, 2005, 124–137.

Vivian I. Binnie. Addressing the topic of smoking cessation in a dental setting. Periodontology 2000, Vol. 48, 2008, 170–178.

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