|
 
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| REVIEW ARTICLE |
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| Year : 2017 | Volume
: 9
| Issue : 1 | Page : 44-51 |
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Smoking and its effect on periodontium – Revisited
Gurparkash Singh Chahal1, Kamalpreet Chhina2, Vipin Chhabra2, Amna Chahal3
1 Department of Periodontology and Implantology, Dr. Harvansh Singh Judge Institute of Dental Sciences and Hospital, Panjab University, Chandigarh, India
2 Department of Periodontology and Implantology, BRS Dental College and Hospital, Panchkula, Haryana, India
3 Private Practioner, Chahal Dental Clinic, Chandigarh, India
| Date of Web Publication | 6-Mar-2017 |
Correspondence Address:
Gurparkash Singh Chahal
150, Sector 11-A, Chandigarh - 161 011
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/IJDS.IJDS_96_16
Cigarette smoking represents a major preventable cause of human disease. Smokers have significantly elevated risks of all-cause mortality and developing a variety of pathological conditions. A direct causal relationship between smoking exposure and the prevalence and the severity of periodontal disease has been firmly established. Although the direct cause for periodontitis is oral bacterial infection, smoking is arguably the strongest behavioral risk factor for the incidence and progression of periodontitis. Smoking has a deleterious effect on all the aspects of periodontium. Smokers have been shown to respond less well to nonsurgical as well as surgical therapy than nonsmokers. Based on this evidence, dental health professionals should advise patients about tobacco's negative health effects as well as the benefits of quitting tobacco use, and tobacco cessation counseling should be a part of the armamentarium of the dental office. Keywords: Periodontium, risk factor, smoking
How to cite this article:
Chahal GS, Chhina K, Chhabra V, Chahal A. Smoking and its effect on periodontium – Revisited. Indian J Dent Sci 2017;9:44-51 |
How to cite this URL:
Chahal GS, Chhina K, Chhabra V, Chahal A. Smoking and its effect on periodontium – Revisited. Indian J Dent Sci [serial online] 2017 [cited 2022 Aug 19];9:44-51. Available from: http://www.ijds.in/text.asp?2017/9/1/44/201643 |
| Introduction | |  |
Cigarette smoking represents a major preventable cause of human disease.[1] Tobacco smoke contains over 3800 chemicals, including carbon monoxide, hydrogen cyanide, and reactive oxidizing radicals, and sixty of these chemicals are known or suspected to be carcinogens.[2] Smokers have significantly elevated risks of all-cause mortality and developing a variety of pathological conditions.[1] A direct causal relationship between smoking exposure and the prevalence and the severity of periodontal disease has been firmly established (American Academy of Periodontology 1996, Grossi et al. 1994).[3],[4] According to the National Health and Nutrition Examination Survey III, 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. The use of tobacco products, in general, and smoking products, in particular, is the major preventable risk factor for the initiation and progression of periodontal diseases.[5],[6],[7] A meta-analysis of data from six such studies involving 2361 individuals indicated that current smokers were nearly three times more likely to have severe periodontitis than nonsmokers. The detrimental impact of long-term smoking on the periodontal and dentate status of older adults has been clearly demonstrated.[8] The most marked difference between smokers and nonsmokers in probing depths or attachment loss occurs in the maxillary lingual area and mandibular anterior teeth, suggesting a local effect of smoking.[9]
It has also been firmly established that smoking cessation is associated with decreased mortality, lower risk of developing a variety of diseases, and increased life expectancy.[1]
| Clinical Parameters of Periodontium Affected by Smoking | | |
Gingival diseases
Gingivitis
Several cross-sectional investigations have indicated that smokers may present with lower levels of gingival inflammation to a specific level of plaque than nonsmokers. This was evidenced using both the gingival index and the dichotomous evaluation of bleeding on probing.[1] Nair et al. followed 27 individuals for 4–6 weeks during a verified successful period of quitting smoking and found bleeding doubled (from 16% to 32%) during this period.[10]
Acute necrotizing ulcerative gingivitis
Pindborg (1947) was one of the first investigators to study the relationship between smoking and periodontal disease. He determined that tar in the smoke exerted a direct irritating effect on the gingiva giving rise to gingivitis and that nicotine could cause contraction of the capillaries, thus interfering with the nutrition of the gingiva which consequently became less resistant to infection.[11]
Periodontitis
Smokers have a higher proportion of sites with deeper probing depths and clinical attachment loss compared with nonsmokers.[4],[12],[13] The observed effects have been confirmed in different studies and in different populations after correcting for a variety of potential confounders.[14]
Cigarette smoking as a risk factor for periodontitis
Although the direct cause for periodontitis is oral bacterial infection, its progression and severity depend on a number of genetic and environmental factors.[14] Several epidemiological studies in different population demonstrate a relationship between smoking and periodontal disease.[15],[16] Cigarette smoking is arguably the strongest behavioral risk factor for the incidence and progression of periodontitis.[17] It is also important to note that although nonsmokers universally respond better to periodontal treatment than do smokers, there is nevertheless substantial evidence of clinical improvement in smokers after treatment, indicating that smoking as a risk factor will compromise rather than prevent tissue healing.[18] Some of the mechanisms by which smoking affects periodontitis are elucidated in [Table 1].[19] | Table 1: How smoking alters the etiology and pathogenesis of periodontal disease
Click here to view |
| Effect of Smoking on the Microbiology of Periodontitis | | |
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 is due to a qualitative rather than quantitative alteration in the plaque.
Several studies report a similar microbial profile of dental plaque in smokers compared with nonsmokers with regard to the ability to detect suspected periodontal pathogens in the subgingival plaque biofilm.[20],[21],[22] However, in smokers, such suspected periodontal pathogens are recovered in shallower areas without clinical periodontal breakdown.[23] More recent studies that utilize molecular techniques capable of characterizing previously unknown bacteria or those that are difficult to culture have provided evidence of distinct microbial profiles and patterns of biofilm colonization in smokers and nonsmokers.[24],[25]
Winkelhoff and Tijhof [26] compared the subgingival microflora of treated and untreated smokers and nonsmokers. They found the most pronounced microbiological characteristics of smokers appeared to be the presence of Bacteroides forsythus, Peptostreptococcus micros, Fusobacterium nucleatum, and Campylobacter rectus in the absence of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. In addition, these pathogenic bacteria were more prevalent in the maxilla than the mandible.[27]
| Impact of Smoking on the Physiology | | |
The clinical signs of inflammation are less pronounced in smokers when compared with nonsmokers. 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 when compared with nonsmokers.[28] Fewer crevicular polymorphonuclear neutrophils (PMNs) and less crevicular phagocytosis could conceivably decrease the release of lysosomal enzymes and thus decrease the level of inflammation in the superficial layers of the periodontal tissues. Smoking-induced chronic hypoxia of periodontal tissues causes greater severity of periodontal disease seen in smokers.[29] Trikilis et al. found that subgingival temperatures are lower in smokers than nonsmokers. The decreased subgingival temperature in smokers might reflect the reduced activity of periodontal cell.[30]
Tobacco and some of its components such as nicotine have been found to have adverse effects on cells of the periodontium, including gingival fibroblasts and cells of the immune system. An in vitro study done by Tanur et al. showed that the nature of cell attachment to root surfaces is altered by nicotine.[31] Cigarette smoke condensate may interfere in myofibroblastic differentiation. Results of the study by Silva et al. showed that cigarette smoke, but not nicotine, may significantly alter cell viability, cell migration, and myofibroblastic differentiation in gingival mesenchymal cells.[32]
Nicotine also caused a dose-dependent inhibition of fibronectin and Type I collagen production. The inhibition of collagen production by nicotine was accompanied by ~700 and 400% increase in collagenase activity at nicotine concentrations of 0.075% and 0.05%, respectively. Nicotine may stimulate transcription of the collagenase gene, either directly or through inducing the production of cytokines by the fibroblasts themselves.
| Impact of Smoking on Immunology | | |
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 immune response, or a combination of both elements.[33] A number of studies have shown that cigarette smoking may affect the host response by altering the immune response in local tissue.[8] Smoke exposure impairs f-actin kinetics, resulting in the damage of the neutrophil cytoskeleton (Ryder et al. 1998).[33]
Effect on oral polymorphonuclear neutrophils
Neutrophils, obtained from the peripheral blood or saliva of smokers, have been shown to demonstrate functional alterations in chemotaxis, phagocytosis, and oxidative burst.[34],[35] One possible mechanism for this elevated neutrophil-mediated destruction may simply be the elevation of neutrophils in smokers seen in the peripheral blood which may lead to increased secretion of potentially tissue-destructive products. In addition, nicotine may prolong the lifespan of neutrophils in tissue by delaying the process of programmed cell death (apoptosis).[36]
Effect on monocytes
The effects of nicotine on monocytes were not restricted to inhibition of the production of oxygen radicals. It also interfered with secretion of the pro-inflammatory cytokine, interleukin 1β (IL-1β). In periodontitis, IL-1β activates fibroblasts and osteoclasts to destroy the periodontal ligament and the alveolar bone. Eventually, the immune response to prolonged infection by periodontal pathogens would overwhelm any short-term anti-inflammatory effect of nicotine.[37]
Effect on circulating polymorphonuclear neutrophils
Circulating PMNs from smokers have been shown to have normal phagocytosis but depressed chemotaxis when testing is performed rapidly after cigarette smoking. This effect is lost after overnight abstinence from smoking, suggesting the presence of a labile substance.[38]
Effect on antibody and lymphocyte response
Nicotine and the water-soluble fraction from whole cigarette smoke can suppress the in vitro secondary antibody response.[39] Salivary immunoglobulin A has been found to be significantly decreased in smokers when compared with nonsmokers.[40] Production of antibody essential for phagocytosis and killing of bacteria, specifically IgG2 levels to periodontal pathogens, has been reported to be reduced in smokers versus nonsmokers with periodontitis.[41]
Effect on cytokines, growth factors, and other enzymes
Elevated levels of tumor necrosis factor-α, prostaglandin-E2, neutrophil elastase, and matrix metalloproteinase-8 have been demonstrated in the gingival crevicular fluid (GCF) of smokers.[41] Wendell et al. demonstrated that nicotine can directly stimulate human gingival fibroblast IL-6 and IL-8 production in vitro. In addition, combination of nicotine and lipopolysaccharide had a synergistic response, upregulating inflammatory cytokine production.[42] IL-4 production by peripheral blood mononuclear cells of smokers was significantly higher than that of nonsmokers (Byron et al. 1994).[43] Bergstrom et al. (2001) observed that for patients with periodontitis, the concentration as well as the total amount of GCF, α-2-macroglobulin and α-1-antitrypsin, was lower in smokers as compared to nonsmokers, which led to increased tissue damage due to increased activity of elastase and collagenase.[44]
| How Smoking Effects the Response to Periodontal Therapy | | |
Nonsurgical therapy
The majority of clinical research supports the observation that pocket depth reduction is more effective in nonsmokers than in smokers using nonsurgical periodontal therapy, including oral hygiene instruction, scaling, and root planing. In addition, gains in clinical attachment as a result of scaling and root planing are less pronounced in smokers than in nonsmokers.[45],[46],[47],[48],[49],[50],[51] Wan et al. found that at 12 months after nonsurgical therapy, smokers presented with a significantly higher percentage of residual pockets. In addition, smokers showed less probing pocket depth (PPD) reduction in sites with initial PPD ≥5 mm.[52] The inhibitory effect of smoking on treatment response is more pronounced at initially deeper sites.[53]
Studies by Preber and Bergström, Grossi et al. (1997),[47] Renvert et al., Machtei et al., and Jin et al. have shown that probing depth reduction and clinical attachment level improvement in smokers are 50%–75% those of nonsmokers, following nonsurgical and surgical therapy.[47],[53],[54],[55],[56],[57] Darby et al. found that nonsmokers with aggressive periodontitis had significantly greater probing depth reduction (2.4 mm) compared with patients with aggressive periodontitis who smoke (1.3 mm).[58]
It can be concluded that smokers respond less well to nonsurgical therapy than nonsmokers. However, in the presence of excellent plaque control, these differences may be minimized.[8]
Antimicrobial therapy
In a 9-month, placebo-controlled, randomized trial in which smokers and nonsmokers were treated by scaling and root planing with and without sub-antimicrobial doxycycline, Preshaw et al. concluded that adjunctive sub-antimicrobial dose doxycycline enhanced therapeutic outcomes in all groups with smokers taking doxycycline, showing approximately the same magnitude of clinical improvement as nonsmokers on placebo.[18],[59] On the other hand, in studies where adjunctive systemic amoxicillin and metronidazole [60] or locally delivered minocycline microspheres [61] enhanced the results of mechanical therapy, there was a greater difference between the control and experimental treatments within smokers as compared to within nonsmokers. These enhanced results might be due to antimicrobial actions, and, in the case of tetracycline derivatives, anticollagenase activity.[3]
Unique regimens that sequence systemic antimicrobial therapy or combine local antimicrobial delivery with host modulatory therapy might offer clinicians and patients options that address microbial and host response alterations in smokers.[62]
Surgical therapy and soft and hard tissues grafting
The clinical benefit seen in nonsmokers following nonsurgical therapy has also been observed following surgical treatment (Ah et al. 1994).[9],[63] The most impressive report of clinical attachment gain in nonsmokers (5.2 mm) compared with smokers (2.1 mm) was observed by Tonetti et al., who carried out guided tissue regeneration (GTR) of infrabony defects using Gore-Tex membranes and with a follow-up period of 1 year. They also concluded that higher plaque levels that are seen consistently in smokers compared with nonsmokers will also have influenced the clinical outcomes.[64]
Smoking is detrimental to regenerative therapy in interproximal and furcation defects, whether treatment includes osseous grafts alone, membranes alone, or membranes in combination with osseous grafts. Studies by Trombelli et al.[65] and Mayfield et al. (1998) reported that evaluated osseous changes by sound probing or re-entry, vertical bone gain in smokers ranged from 0.1 to 0.5 mm, whereas nonsmokers demonstrated 0.9–3.7 mm improvement.[66] Stavropoulos et al. showed that smoking exerted a detrimental effect on the outcome of GTR treatment of intrabony defects with bioresorbable membranes.[67]
When expanded polytetrafluoroethylene membranes were utilized in GTR procedures at recession sites, smokers had significantly less root coverage (57%) as compared to nonsmokers (78%).[68] The superior blood supply afforded by the subepithelial connective tissue graft might be more resistant to the effects of smoking as compared to the nonresorbable barrier membrane.[3] However, root coverage following thick free gingival graft procedures is reportedly diminished by heavy cigarette smoking and there are conflicting reports on smoking's effect on the success of subepithelial connective tissue grafts.[68]
Implant therapy
Based on a multivariate statistical model adjusted for age, gender, and jaw position, smoking is significantly associated with implant failure.[10] In the studies reviewed, 0%–17% of implants placed in smokers were reported as failures as compared to 2%–7% in nonsmokers, with the majority of studies showing at least twice as many failed implants in smokers.[3]
The largest data set on the influence of smoking on implant success comes from the Dental Implant Clinical Research Group (DICRG) of the Department of Veterans Affairs, which is an 8-year, randomized, prospective clinical study that includes >2900 implants.[69] The 3-year data demonstrated that 8.9% of implants placed in smokers failed as compared to 6% in individuals who had never smoked or had quit smoking. The majority of implant failures in smokers occurred before prosthesis delivery; thereafter, the differences between smokers and nonsmokers tended to disappear.[70]
Several investigators have confirmed that smoking more negatively impacts implants placed in the maxillary arch than in the mandible. The DICRG reported that the percentage of maxillary implant failures among smokers (10.9%) was almost twice that reported for nonsmokers or past smokers (6.4%).[69]
The majority of the existing reports deal with machined titanium surfaces, and early evidence suggests that the currently, more popular roughened surfaces can partially compensate for the negative healing response in smokers.[3] A meta-analysis done by Bain reported that light smoking (average of 12 cigarettes/day) did not affect the success rate of either machined or dual acid-etched surface implants.[71]
Implant therapy in grafted sites
Emerging data indicate that the impact of smoking on implant therapy is more dramatic in grafted maxillary sinuses compared to nongrafted sites. The percentage of implant failures in grafted sinuses in smokers is 1.4–3.9 times greater than that of nonsmokers, with the majority of studies showing at least 2.5 times the number of failed implants in smokers.[3]
| Impact of Smoking Cessation on Periodontal Status and Treatment Outcomes | | |
There was no association between number of years since cessation of smoking and changes in mean pocket depth or clinically attachment loss in former smokers. The negative effect of smoking on the subgingival environment and flora appears to be reversible. This is evidenced by the fact that a comparable proportion of former and nonsmokers became negative for P. gingivalis and B. forsythus after mechanical treatment.[47]
In the only longitudinal study to date, Preshaw et al. have reported 12-month data from 10 individuals with periodontitis who quit smoking. The quitters demonstrated a significant reduction in probing depths compared with nonquitters as well as a higher incidence of probing depth reductions of ≥3 mm.[72] Further, the implementation of population-based smoking cessation programs may also have a significant impact on the prevalence and progression of periodontal diseases (Susin et al. 2004).[73]
| Tobacco Counseling – A Component of Periodontal Therapy | | |
Nicotine dependence is classified as a chemical addiction by the American Psychiatric Association in the Diagnostic and Statistical Manual of Mental Disorders, 1994 (IV). A useful model brief intervention that uses a five-step approach is recommended by the Agency for Health Care Research and Quality [Table 2].[74],[75]
If a patient has expressed a sincere interest in quitting, the chances of success are far greater than if the patient is unwilling to quit or wishes to postpone the start of a cessation program. For these patients, before deciding whether to proceed with a smoking cessation program, a Five R's approach has been developed [Table 3].[76],[77]
Success is most likely to be achieved when counseling and pharmacological approaches, such as nicotine-replacement therapies [Table 4], are used in combination.[76],[78]
| Conclusion | | |
With a growing smoking prevalence, the proportion of tobacco-attributed disease will probably contribute comparably more to total periodontal disease in future years.[10] The American Academy of Periodontology Parameters of Care include tobacco cessation as a part of periodontal therapy and the 2000 Surgeon General's Report on Oral health in America encourage dental professionals to become more active in tobacco cessation counseling.[3]
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Tonetti MS. Cigarette smoking and periodontal diseases: Etiology and management of disease. Ann Periodontol 1998;3:88-101.  |
| 2. | Eriksen MP, LeMaistre CA, Newell GR. Health hazards of passive smoking. Annu Rev Public Health 1988;9:47-70. |
| 3. | Johnson GK, Hill M. Cigarette smoking and the periodontal patient. J Periodontol 2004;75:196-209. |
| 4. | Grossi SG, Zambon JJ, Ho AW, Koch G, Dunford RG, Machtei EE, et al. Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J Periodontol 1994;65:260-7. |
| 5. | Genco RJ, Borgnakke WS. Risk factors for periodontal disease. Periodontol 2000 2013;62:59-94. |
| 6. | Johnson GK, Guthmiller JM. The impact of cigarette smoking on periodontal disease and treatment. Periodontol 2000 2007;44:178-94. |
| 7. | Nociti FH Jr., Casati MZ, Duarte PM. Current perspective of the impact of smoking on the progression and treatment of periodontitis. Periodontol 2000 2015;67:187-210. |
| 8. | Novak MJ, Novak KF. Smoking and periodontal disease. Clinical Periodontology. 10 th ed. St. Louis, Mo.: Saunders Elsevier, 2006. p. 251-8. |
| 9. | Trombelli L, Cho KS, Kim CK, Scapoli C, Scabbia A. Impaired healing response of periodontal furcation defects following flap debridement surgery in smokers. A controlled clinical trial. J Clin Periodontol 2003;30:81-7. |
| 10. | Nair P, Sutherland G, Palmer RM, Wilson RF, Scott DA. Gingival bleeding on probing increases after quitting smoking. J Clin Periodontol 2003;30:435-7. |
| 11. | Pindborg JJ. Tobacco and gingivitis I. Statistical examination of the significance of tobacco in the development of ulceromembranous gingivitis and in the formation of calculus. J Dent Res 1947; 26:261. |
| 12. | Eke PI, Dye BA, Wei L, Slade GD, Thornton-Evans GO, Borgnakke WS, et al. Update on Prevalence of Periodontitis in Adults in the United States: NHANES 2009 to 2012. J Periodontol 2015;86:611-22. |
| 13. | Martinez-Canut P, Lorca A, Magán R. Smoking and periodontal disease severity. J Clin Periodontol 1995;22:743-9. |
| 14. | Genco RJ. Current view of risk factors for periodontal diseases. J Periodontol 1996;67 10 Suppl:1041-9. |
| 15. | Haber J, Wattles J, Crowley M, Mandell R, Joshipura K, Kent RL. Evidence for cigarette smoking as a major risk factor for periodontitis. J Periodontol 1993;64:16-23. |
| 16. | Schenkein HA, Gunsolley JC, Koertge TE, Schenkein JG, Tew JG. Smoking and its effects on early-onset periodontitis. J Am Dent Assoc 1995;126:1107-13. |
| 17. | Walter C, Kaye EK, Dietrich T. Active and passive smoking: Assessment issues in periodontal research. Periodontol 2000 2012;58:84-92. |
| 18. | Heasman L, Stacey F, Preshaw PM, McCracken GI, Hepburn S, Heasman PA. The effect of smoking on periodontal treatment response: A review of clinical evidence. J Clin Periodontol 2006;33:241-53. |
| 19. | Malhotra R, Kapoor A, Grover V, Kaushal S. Nicotine and periodontal tissues. J Indian Soc Periodontol 2010;14:72-9. [ PUBMED]  |
| 20. | Apatzidou DA, Riggio MP, Kinane DF. Impact of smoking on the clinical, microbiological and immunological parameters of adult patients with periodontitis. J Clin Periodontol 2005;32:973-83. |
| 21. | Boström L, Bergström J, Dahlén G, Linder LE. Smoking and subgingival microflora in periodontal disease. J Clin Periodontol 2001;28:212-9. |
| 22. | Darby IB, Hodge PJ, Riggio MP, Kinane DF. Microbial comparison of smoker and non-smoker adult and early-onset periodontitis patients by polymerase chain reaction. J Clin Periodontol 2000;27:417-24. |
| 23. | Eggert FM, McLeod MH, Flowerdew G. Effects of smoking and treatment status on periodontal bacteria: Evidence that smoking influences control of periodontal bacteria at the mucosal surface of the gingival crevice. J Periodontol 2001;72:1210-20. |
| 24. | Kumar PS, Matthews CR, Joshi V, de Jager M, Aspiras M. Tobacco smoking affects bacterial acquisition and colonization in oral biofilms. Infect Immun 2011;79:4730-8. |
| 25. | Ramseier CA, Fundak A. Tobacco use cessation provided by dental hygienists. Int J Dent Hyg 2009;7:39-48. |
| 26. | Winkelhoff V, Tijhof B. Effects of smoking on subgingival microflora. J Periodontol 2001;72:666-71. |
| 27. | Haffajee AD, Socransky SS. Relationship of cigarette smoking to the subgingival microbiota. J Clin Periodontol 2001;28:377-88. |
| 28. | Bergström J, Preber H. Tobacco use as a risk factor. J Periodontol 1994;65 5 Suppl:545-50. |
| 29. | Rivera-Hidalgo F. Smoking and periodontal disease. A review of the literature. J PEriodontol 1986;57:617-24. |
| 30. | Trikilis N, Rawlinson A, Walsh TF. Periodontal probing depth and subgingival temperature in smokers and non-smokers. J Clin Periodontol 1999;26:38-43. |
| 31. | Tanur E, McQuade MJ, McPherson JC, Al-Hashimi IH, Rivera-Hidalgo F. Effects of nicotine on the strength of attachment of gingival fibroblasts to glass and non-diseased human root surfaces. J Periodontol 2000;71:717-22. |
| 32. | Silva D, Cáceres M, Arancibia R, Martínez C, Martínez J, Smith PC. Effects of cigarette smoke and nicotine on cell viability, migration and myofibroblastic differentiation. J Periodontal Res 2012;47:599-607. |
| 33. | Bergström J. Tobacco smoking and risk for periodontal disease. J Clin Periodontol 2003;30:107-13. |
| 34. | Ryder MI, Fujitaki R, Johnson G, Hyun W. Alterations of neutrophil oxidative burst by in vitro smoke exposure: Implications for oral and systemic diseases. Ann Periodontol 1998;3:76-87. |
| 35. | Kenney EB, Kraal JH, Saxe SR, Jones J. The effect of cigarette smoke on human oral polymorphonuclear leukocytes. J Periodontal Res 1977;12:227-34. |
| 36. | Pabst MJ, Pabst KM, Collier JA, Coleman TC, Lemons-Prince ML, Godat MS, et al. Inhibition of neutrophil and monocyte defensive functions by nicotine. J Periodontol 1995;66:1047-55. |
| 37. | Noble RC, Penny BB. Comparison of leukocyte count and function in smoking and nonsmoking young men. Infect Immun 1975;12:550-5. |
| 38. | Roszman TL, Rogers AS. The immunosuppressive potential of products derived from cigarette smoke. Am Rev Respir Dis 1973;108:1158-63. |
| 39. | Bennet KR, Reade PC. Salivary immunoglobulin a levels in normal subjects, tobacco smokers, and patients with minor aphthous ulceration. Oral Surg Oral Med Oral Pathol 1982;53:461-5. |
| 40. | Tangada SD, Califano JV, Nakashima K, Quinn SM, Zhang JB, Gunsolley JC, et al. The effect of smoking on serum IgG2 reactive with Actinobacillus actinomycetemcomitans in early-onset periodontitis patients. J Periodontol 1997;68:842-50. |
| 41. | Soder B. Neutrophil elastase activity, levels of prostaglandin E2, and matrix metalloproteinase-8 in refractory periodontitis sites in smokers and nonsmokers. Acta Odontol Scand 1999;57:77. |
| 42. | Wendell KJ, Stein SH. Regulation of cytokine production in human gingival fibroblasts following treatment with nicotine and lipopolysaccharide. J Periodontol 2001;72:1038-44. |
| 43. | Byron KA, Vaigos GA, Wooton AM. IL- 4 production is increased in cigarette smokers. CLinical Experimental Immunology 2004;95:333-6. |
| 44. | Persson L, Bergstrom J, Ito H, Gustaffson A. Tobacco smoking and neutrophil activity in patients with periodontal disease. J Periodontol 2001;72:90-5. |
| 45. | Ah MK, Johnson GK, Kaldahl WB, Patil KD, Kalkwarf KL. The effect of smoking on the response to periodontal therapy. J Clin Periodontol 1994;21:91-7. |
| 46. | Grossi SG, Skrepcinski FB, DeCaro T, Zambon JJ, Cummins D, Genco RJ. Response to periodontal therapy in diabetics and smokers. J Periodontol 1996;67 10 Suppl:1094-102. |
| 47. | Grossi SG, Zambon J, Machtei EE, Schifferle R, Andreana S, Genco RJ, et al. Effects of smoking and smoking cessation on healing after mechanical periodontal therapy. J Am Dent Assoc 1997;128:599-607. |
| 48. | Haffajee AD, Cugini MA, Dibart S, Smith C, Kent RL Jr., Socransky SS. The effect of SRP on the clinical and microbiological parameters of periodontal diseases. J Clin Periodontol 1997;24:324-34. |
| 49. | Kaldahl WB, Johnson GK, Patil KD, Kalkwarf KL. Levels of cigarette consumption and response to periodontal therapy. J Periodontol 1996;67:675-81. |
| 50. | Quinn SM, Zhang JB, Gunsolley JC, Schenkein HA, Tew JG. The influence of smoking and race on adult periodontitis and serum IgG2 levels. J Periodontol 1998;69:171-7. |
| 51. | Renvert S, Dahlen G, Wikstrom M. The clinical and microbiologic effects of non-surgical periodontal therapy in smokers and nonsmokers. J Clin Periodontol 1998;25:153. |
| 52. | Wan CP, Leung WK, Wong MC, Wong RM, Wan P, Lo EC, et al. Effects of smoking on healing response to non-surgical periodontal therapy: A multilevel modelling analysis. J Clin Periodontol 2009;36:229-39. |
| 53. | Kinane DF, Radvar M. The effect of smoking on mechanical and antimicrobial periodontal therapy. J Periodontol 1997;68:467-72. |
| 54. | Preber H, Bergström J. The effect of non-surgical treatment on periodontal pockets in smokers and non-smokers. J Clin Periodontol 1986;13:319-23. |
| 55. | Renvert S, Dahlén G, Wikström M. The clinical and microbiological effects of non-surgical periodontal therapy in smokers and non-smokers. J Clin Periodontol 1998;25:153-7. |
| 56. | Machtei EE, Hausmann E, Schmidt M, Grossi SG, Dunford R, Schifferle R, et al. Radiographic and clinical responses to periodontal therapy. J Periodontol 1998;69:590-5. |
| 57. | Jin L, Wong KY, Leung WK, Corbet EF. Comparison of treatment response patterns following scaling and root planing in smokers and non-smokers with untreated adult periodontitis. J Clin Dent 2000;11:35-41. |
| 58. | Darby IB, Hodge PJ, Riggio MP, Kinane DF. Clinical and microbiological effect of scaling and root planing in smoker and non-smoker chronic and aggressive periodontitis patients. J Clin Periodontol 2005;32:200-6. |
| 59. | Preshaw PM, Hefti AF, Bradshaw MH. Adjunctive subantimicrobial dose doxycycline in smokers and non-smokers with chronic periodontitis. J Clin Periodontol 2005;32:610-6. |
| 60. | Winkel EG, Van Winkelhoff AJ, Timmerman MF, Van der Velden U, Van der Weijden GA. Amoxicillin plus metronidazole in the treatment of adult periodontitis patients. A double-blind placebo-controlled study. J Clin Periodontol 2001;28:296-305. |
| 61. | Williams RC, Paquette DW, Offenbacher S, Adams DF, Armitage GC, Bray K, et al. Treatment of periodontitis by local administration of minocycline microspheres: A controlled trial. J Periodontol 2001;72:1535-44. |
| 62. | Novak MJ, Johns LP, Miller RC, Bradshaw MH. Adjunctive benefits of subantimicrobial dose doxycycline in the management of severe, generalized, chronic periodontitis. J Periodontol 2002;73:762-9. |
| 63. | Ah MK, Johnson GK, Kaldahl WB, Patil KD, Kalwarf KL. The effect of smoking on the response to periodontal therapy. J Clin Periodontol 1994;21:91-7. |
| 64. | Trombelli L, Kim CK, Zimmerman GJ, Wikesjö UM. Retrospective analysis of factors related to clinical outcome of guided tissue regeneration procedures in intrabony defects. J Clin Periodontol 1997;24:366-71. |
| 65. | Tonetti MS, Pini-Prato G, Cortellini P. Effect of cigarette smoking on periodontal healing following GTR in infrabony defects. A preliminary retrospective study. J Clin Periodontol 1995;22:229-34. |
| 66. | Mayfield L, Soderholm G, Hallstrom H. Guided tissue regeneration for the treatment of intraosseous defects using bio-absorbable membrane. A controlled clinical study. J Clin PEriodontol 1998;25:585-95. |
| 67. | Stavropoulos A, Mardas N, Herrero F, Karring T. Smoking affects the outcome of guided tissue regeneration with bioresorbable membranes: A retrospective analysis of intrabony defects. J Clin Periodontol 2004;31:945-50. |
| 68. | Trombelli L, Scabbia A. Healing response of gingival recession defects following guided tissue regeneration procedures in smokers and non-smokers. J Clin Periodontol 1997;24:529-33. |
| 69. | American Academy of Periodontology. Tobacco use and the periodontal patient (position paper). J Periodontol 1996;67:51-6. |
| 70. | Lambert PM, Morris HF, Ochi S. The influence of smoking on 3-year clinical success of osseointegrated dental implants. Ann Periodontol 2000;5:79-89. |
| 71. | Bain CA. Implant installation in the smoking patient. Periodontol 2000 2003;33:185-93. |
| 72. | Preshaw PM, Heasman L, Stacey F, Steen N, McCracken GI, Heasman PA. The effect of quitting smoking on chronic periodontitis. J Clin Periodontol 2005;32:869-79. |
| 73. | Susin C, Oppermann RV, Haugejordan O, Albander JM. Periodontal atachment loss attributable to cigarette smoking in urban Brazilian population. J Clin Periodontol 2004;31:951-8. |
| 74. | Fiore M, Jaen CR, Baker TB, Bailey WC, Bennett G, Benowitz N et al. A clinical practical guideline for treating tobacco use and dependence: 2008 Update. A US Public Health Service report. Am J Prev Med 208; 35:158-76. |
| 75. | Walsh MM, Ellison JA. Treatment of tobacco use and dependence:the role of dental professional. J Dent Educ 2005; 69: 521-37. |
| 76. | Fiore MC, Bailey WC, Cohen SJ, Dorfman SF, Fox BJ, Gritz E. et al. Treating Tobacco Use and Dependence. Washington, DC: U.S. Department of Health and Human Services, Public Health Service; 2000. |
| 77. | Chaffee BW, Couch ET, Ryder MI. The tobacco-using periodontal patient: Role of the dental practitioner in tobacco cessation and periodontal disease management. Periodontol 2000 2016;71:52-64. |
| 78. | Stead LF, Perera R, Bullen C, Mant D, Lancaster T. Nicotine replacement therapy for smoking cessation. Cochrane Database Syst Rev 2012; 14:11:CD000146. |
[Table 1], [Table 2], [Table 3], [Table 4]
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