Journal of the International Clinical Dental Research Organization

REVIEW ARTICLE
Year
: 2021  |  Volume : 13  |  Issue : 1  |  Page : 3--9

Role of smoking and its impact on periodontium


Anshul Sawhney1, Megha Ralli2, Shishir Dhar3, Bharat Gupta4, Snehal Sunil Ghodke5, Shamika Purao5,  
1 Department of Dentistry (Periodontology), Maharaja Suhel Dev Medical College and Mahrshi Balark Hospital, Bahraich, Uttar Pradesh, India
2 Department of Pathology, Maharaja Suhel Dev Medical College and Mahrshi Balark Hospital, Bahraich, Uttar Pradesh, India
3 Department of Dentistry, Government Medical College, Saharanpur, Uttar Pradesh, India
4 Department of Periodontology, MGM Dental College, Navi Mumbai, Maharashtra, India
5 Intern MGM Dental College, Navi Mumbai, Maharashtra, India

Correspondence Address:
Dr. Anshul Sawhney
Assistant Professor, Department of Dentistry (Periodontology), Maharaja Suhel Dev Medical College and Mahrshi Balark Hospital, Bahraich, Uttar Pradesh -271 801
India

Abstract

Smoking is 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 as compared with nonsmokers. 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. Several tobacco intervention approaches can be useful in helping the patient deal with the nicotine withdrawal symptoms and psychological factors associated with smoking cessation. In addition, pharmacotherapeutic treatments such as nicotine replacement therapy and sustained bupropion administration have proved effective.



How to cite this article:
Sawhney A, Ralli M, Dhar S, Gupta B, Ghodke SS, Purao S. Role of smoking and its impact on periodontium.J Int Clin Dent Res Organ 2021;13:3-9


How to cite this URL:
Sawhney A, Ralli M, Dhar S, Gupta B, Ghodke SS, Purao S. Role of smoking and its impact on periodontium. J Int Clin Dent Res Organ [serial online] 2021 [cited 2022 Jan 21 ];13:3-9
Available from: https://www.jicdro.org/text.asp?2021/13/1/3/319522


Full Text



 Introduction



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 long-term success of implant placement [Table 1].[1] Currently, smoking is more common among low-income adults (37.1%) compared with medium- or high-income earners and increases with decreasing years of education.[2]{Table 1}

Approximately 25% of the United States population smokes cigarettes,[3] and in other areas of the world, the percentage of smokers is even higher.[4],[5] Depending upon which parameters are used to assess periodontal disease, smokers are 2.6–6 times more likely to develop periodontal disease than nonsmokers.[6] The odds ratio for a moderate smoker (15–30 pack-years) to have periodontal disease is 2.77 times that of a nonsmoker, and the odds ratio for a heavy smoker (≥30 pack-years) is 4.75 times more likely to have periodontal disease than a nonsmoker.[7]

Pack-years can be defined as the number of cigarettes (packs) smoked per day multiplied by the number of years that an individual smoked.

Toxicity of tobacco smoke

The important carcinogens are polycyclic aromatic hydrocarbons and N-nitroso compounds found in the tar residue. Tobacco smoke also contains noxious substances such as benzanthracene and hydrogen cyanide, which undoubtedly have antibacterial properties. Tobacco smoke appears to be selectively bactericidal and as a result produces changes in the oral ecosystem, which among other effects may predispose smokers to increased risk of candidiasis.[8]

Nicotine

Nicotine is considered the most pharmacologically active compound in tobacco smoke. Most is absorbed, though more slowly, through the oral mucosa in sufficient quantities to have a pharmacological effect.[9] Nicotine has structural resemblance to acetylcholine; it blocks acetylcholine by competitive blockade at the autonomic ganglia, initially stimulating and subsequently depressing synaptic transmission as a dose–response effect on the ganglion receptor.

The lethal dose of nicotine can block synaptic transmission altogether. Smoking causes vasoconstriction and increases heart rate, cardiac output leading to increased blood pressure.

Cotinine

Cotinine from smoking was reported to enhance the effects of toxins from periodontopathogens in a chick embryo toxin assay, suggesting a mechanism by which smoking contributes to the severity of periodontal disease.

Acrolein and acetaldehyde

These volatile tobacco smoke components were found to be toxic to cultures of the human gingival fibroblasts, affecting attachment and proliferation in a dose-dependent response. These compounds affect cell adhesion in culture by the disruption of microtubules and associated filaments.

There is increased colonization of shallow periodontal pockets by the periodontal pathogens and increased levels of periodontal pathogens in deep periodontal pockets. There is increased in numbers and virulence of pathogenic organism and also changes in host response. Smokers exhibit depressed number of helper T-lymphocytes, which are important to stimulate B-cell function for antibody production.[10] Neutrophils from smokers with refractory periodontitis exhibit impaired phagocytosis.[11] Nicotine has been shown to decrease the gingival blood flow.[12] Periodontal wound healing may be adversely affected, which may impair revascularization in the soft tissues and hard tissues.[13]

 Mechanisms of Periodontal Disease Progression in Smokers [Table 2]

{Table 2}

The increased prevalence and severity of periodontal destruction associated with smoking suggest that the host bacterial interactions normally seen in chronic periodontitis are altered, resulting in more aggressive periodontal breakdown.[14]

There is decreased GCF flow and bleeding on probing with increased inflammation.[15]

 Effects of Smoking on the Response to Periodontal Therapy



Numerous studies have indicated that current smokers do not respond as well to periodontal therapy as nonsmokers or former smokers.[16],[17]

Therapy

Nonsurgical:

Decreased clinical response to scaling and root planningDecreased reduction in pocket depthDecreased gain in CADecreased negative impact of smoking with increased level of plaque control.

Surgery and implants:

Decreased pocket depth reduction postsurgeryIncreased deterioration of furcation postsurgeryDecreased gain on clinical attachment levelsDecreased bone fill, increase recession.

Increased membrane exposure following GTR:

Decreased pocket depth reduction after DFDBA allograftsDecreased pocket depth reduction and gain in CAL after open flap debridement.Conflicting data on the impact of smoking on implant successSmoking cessation should be recommended before implants.

Maintenance:

Increased pocket depth during maintenanceDecreased gain in CAL.

Recurrent (refractory):

Increased recurrent/refractory disease in smokers diseaseIncrease for retreatment in smokersIncreased need for antibiotics in smokers to control the negative effects of periodontal infection on surgical outcomesIncreased tooth loss in smokers after surgical therapy.

Mechanism of action of Nicotine on polymorphoneutrophills(PMN'S) [Table 2]

Smoking exerts major effects on the protective immune response, and the neutrophil is an important component of host response. It plays an important role in chemotaxis, phagocytosis, and killing using oxidative and nonoxidative mechanism. Neutrophils obtained from the oral cavity of smokers or exposed in vitro to nicotine have shown to demonstrate functional alterations in chemotaxis, phagocytosis, and oxidative burst. Superoxide and hydrogen peroxide generation, integrin expression, and protease inhibitor production are also affected. Studies have shown that nicotine exposure increases secretion of prostaglandins by monocytes in response to lipopolysaccharides, resulting in more periodontal destruction; furthermore, antibody production is also reduced which is essential for phagocytosis and the levels of immunoglobulin G2 are also reduced. Nicotine impairs the elimination of periodontal pathogens by inhibiting reactive oxygen species (ROS) release by neutrophils, which results in oxidative stress-mediated tissue damage. Changes in neutrophil morphology and morphometry after smoking that resulted in reduced function and depressed ability to adhere have also been reported. Seow et al.[18] examined the effects of nicotine on neutrophil function at concentration achievable in the oral tissues The results showed a dose-dependent suppression of both chemotaxis and phagocytosis. MacFarlane et al.[19] showed impaired phagocytosis in neutrophils from these subjects. Impaired polymorphonuclear neutrophil (PMN) function may contribute to an increased risk for periodontitis in the later life. Nicotine contributes to disease by several pathways, including stimulation of inflammation. Nicotine has been demonstrated to suppress phagocytic activity in neutrophils while enhancing degranulation as determined by neutrophil elastase release without affecting superoxide production.[20] Nicotine can impair phagocytic host defense while also increasing ROS-associated injury. Nicotine has been shown to block Akt deactivation and reduce spontaneous death of neutrophils.[21]

Tobacco cessation programs and policies

The treating tobacco use and dependence clinical practice guidelines recommend the 5 A's and 5 R's approach should be focused on those patients who are not ready to quit.

Ask about the tobacco useAdvice all users to quitAssess willingness to make a quit attemptAssist the patient to quitArrange follow-up contact.

RelevanceRiskRewardsRoad blocksRepetition.

As we know in India, tobacco-associated mortality is the highest in the world with an annual of 7 lacs death. Tobacco cessation clinics were set up in India by the WHO and the Government of India for tobacco cessation intervention. 31% of total registered cases in the initial years were treated with nicotine gums and behavioral counseling. The abstinence rate was 15%–17% in the counseling group, and it was higher around 53%–60% in the medication group.[22] Variety of nonpharmacological and pharmacological interventions now are available which help in tobacco cessation.

Various approaches in smoking cessation are:

Increased tobacco taxation and counter-marketing campaignsUse of counseling and pharmacotherapyVarious medicines that increase long-term smoking cessation are nicotine inhalers, bupropion SR nicotine lozenge, nicotine patches, nicotine gums, nasal sprays, and vareniclineFirst-line medications are nicotine gums, inhalers, lozenges, and patch. Proven second-line medications are clonidine, nicotine, spray, and nortriptylineAccording to the WHO guidelines, more than one type of pharmacotherapy should be offered in combination if appropriate for a prolonged periodUse of mass reach health communication interventions, e.g., television, radiobroadcasts, newspapers, and billboardsQuit lines can be used as phone-based service. Use of caller tunes for stopping smoking. National call centers should be established to provide counselingTobacco cessation programs should be custom made depending upon income and educational statusNicotine replacement therapy involves the use of other nicotine substitutes. It relieves some of the withdrawal symptoms by delivering small and steady doses of nicotine into your body. This type of treatment helps you focus on breaking your psychological addiction and makes it easier to concentrate on learning new behaviors and coping skills. It involves use of gums, transnsversal patches, nasal sprays, and sublingual tablets. Bupropion (Zyban) and varenicline (Chantix, Champix) are well-known pharmacological interventions, meant for short-term use.

Brand names of nicotine gums

Nicorette 2 mg tablet; Mfg. JOHNSON and JOHNSON; Packet size: 1 pieceNicotex 2 mg chewing gum; Mfg. CIPLA; Packet size: 9 piecesNicogum 4 mg; Mfg. CIPLA; Packet size: 10 piecesEucomint 2 mg tablet; Mfg. ELDER; Packet size: 20 pieces.

Alternative therapies such as use of yoga, hypnosis, herbal products, acupuncture, relaxation, and massage therapy. Behavior therapy focuses on learning new coping skills and breaking those habits. Some people have been able to find the motivation to quit just by calculating how much money they will saveNicotine vaccines present a new approach but are still under investigation. Nicotine-based vaccines can prime the immune system to recognize nicotine as foreign and to mount an immune response against the drug. In doing so, vaccines may reduce the nicotine being absorbed in brain. E.g., NicVax (bacterial exoprotein conjugate vaccine), Nic 002 (Nicotine Q beta), TA-NIC (a recombinant cholera toxin conjugate vaccine), SEL-068[23],[24]Use of electronic cigarettes which are battery-operated electronic device that is designed to vaporize a liquid solution, known to contain propylene glycol and/or vegetable glycerin in which nicotine or other fragrances may be dissolved. It delivers nicotine through inhaling vapors. No sufficient studies to demonstrate vapors generated from e-cigarettes do not contain any toxic substance. E cigarettes are banned in various countries like Canada, Mexico, Israel, HongKong, Singapore and UAE.

Mass population policies through government support aimed in designing of policies to help smokers who are already motivated to quit the habit. Along with educational campaigns, increased taxations and restrictions on smoking in public places will help in people quiit the habit of smoking.

Influence of smoking on long-term success of implants

The risk factors for implant are due to surgical procedure (type of implant, location, time lapse between tooth removal and implant placement, and loading) as well as patient characteristics such as smoking, oral hygiene, uncontrolled diabetes, and alcohol consumption. Success rate of implant depends on many factors including oral hygiene, operator skill, implant material (type and length) used, bone quality and quantity, occlusal load, and presence of any medical condition. Smoking has a strong influence on the complication rates of implants. It causes more marginal bone loss after implant placement and also increases the incidence of peri-implantitis. The failure rate of implants placed in the grafted maxillary sinuses of smokers is more than twice as seen in nonsmokers. Cigarette smoking may have cytotoxic effects on the gingival fibroblasts, which results in decreased capacity for proliferation and binding capacity.[25] The cutaneous vasoconstrictive action of nicotine, compromised PMN leukocyte function, increased platelet adhesiveness, increased levels of fibrinogen and hemoglobin, as well as increased blood viscosity have been hypothesized mechanisms by which smoking contributes to altered wound-healing mechanism.[26],[27],[28],[29],[30] The exact mechanisms by which smoking affects implant failure is still not understood; however, it affects cell differentiation of pluripotent mesenchymal cells into osteoblast and fibroblast, leading to impaired healing of bone around implant interface. Out of the various bioactive compounds, nicotine plays a critical role in affecting bone healing. Nicotine permeability of the gingival epithelium around implants is very high, so the osteoblastic activity is impaired. Smoking also affects osseointegration by lowering blood flow rate due to platelet aggregation and increase in the peripheral resistance as well. Smoking also increases chances of infection at implant by decreasing proliferation of macrophages as well as defensive mechanisms of neutrophils.

Various authors who conducted long-term studies of effect of smoking on success rate of implants

Brain and Moy were the first to evaluate the influence of smoking on the failure rate of implants. When patients were subdivided into smokers and nonsmokers, it was found that a significantly greater percentage of failures occurred in smokers (11.28%) than in nonsmokers (4.76%) (P < 0.001). The findings of this study, for the first time, identified smoking as a major factor in implant failure.[31] When patients were subdivided into smokers and nonsmokers, it was found that a significantly greater percentage of failures occurred in smokers (11.28%) than in nonsmokers (4.76%) (P < 0.001). The findings of this study, for the first time, identified smoking as a major factor in implant failure. A smoking cessation protocol was put in place by Bain[32] in 1997, and he found through his study that there was a statistically significant difference in the failure rates between those who continued to smoke and those who were on the protocol. Because all failures occurred before prosthetic loading, they were not likely to be a result of prosthodontic overload or other external factorsOther studies[33] have also identified tobacco use as one of the statistically significant (P = 0.004) factors associated with an increased risk of implant failure, with a hazard ratio of 4.3, i.e., the risk of implant failure in smokers is 4.3 times that in nonsmokersGorman et al.,[34] in their study of patients who had received over 2000 implants, found significantly more failures in smokers after second-stage surgeryLambert et al.[35] also conducted a longitudinal study to assess the influence of smoking in a group of patients with over 2900 endosteal dental implants. The results did not show the expected early failure after the initial surgery but showed more failures after the second-stage of surgery. The authors theorized that the effect of tobacco on healing after implant placement was different from that after tooth extraction, because implant wounds were closed and the intimate adaptation of the implant to the bone tissue did not allow the same magnitude of interference in healing by the vasoconstrictive action of nicotineAfter the implants were uncovered, the soft tissues around them were adversely affected by tobacco in a manner similar to that by which periodontal tissues were adversely affected. In another retrospective cohort study,[36] the risk factors for implant failure were determined by evaluating a total of 4680 implants placed in 1140 patients over a 21-year period from 1982 to 2003. Most of the subjects were followed up over 20 years. Smoking was found to be a significant predictor of implant failure, with a relative risk of 1.56 (P = 0.03). Most of the failures occurred within the 1st year, with very few failing at later time points. Patients who disclosed a history of smoking had a failure rate of 20%. Implants placed within the maxilla experienced almost twice the failure rate of those placed in the mandible (P < 0.001). Implants placed in the anterior mandible had the lowest failure rate of any location. Advanced age increased the risk of implant failure: patients older than 60 years were twice as likely to have adverse outcomesBezerra Ferreira et al. concluded that cigarette smoking has a significant role on early bone tissue response around sandblasted acid-etched implant surface.[37]

Main outcomes of these studies are

Implant failure was more among smokers compared to nonsmokersHigher implant failure with increased cigarette smoking frequency (>20 packets/day)Increased risk with increased duration of smoking (over 10 years of duration) [Table 1].

Studies which did not support effect of smoking on long-term success of implants

Galindo-Moreno et al.[38] conducted a prospective clinical study to explore the possible link between peri-implant bone loss and the widespread habits of tobacco smoking and alcohol consumption. Although tobacco is described in the literature as one of the most influential etiological agents in peri-implant marginal bone loss, it did not appear to play such an important role in the present studyGrunder et al.[39] also found no significant difference in implant failures between smokers and nonsmokers. Some other smaller studies have also failed to find a link between smoking and implant failures[40]Based on the above reviews, it is mandatory to instruct the patient and take a proper history before any procedure

The smoking history should first be obtained; this should include the duration of smoking, the intensity (past and present) and the present status. It is especially important to identify former heavy smokers who have recently stoppedAppropriate oral hygiene instructions should be given and the deleterious effects of smoking on oral hygiene should be highlighted, with special mention made of the effect of smoking as a risk factor for periodontal disease. The periodontal status of the patient is also a valuable indicator of the prognosisThe patient should then be advised of the poor prognosis of implants in smokers, especially in the maxillary region. Increasing the predictability of the success of dental implants is one strong reason why patients should be advised to stop smoking permanently. The decision to proceed with implant treatment has to be made by a clinician depending upon the number of cigarettes smoked, the risk of failure, etc.Informed consent plays a very important role with the clinician explaining all the facts and getting the patient's signature on the appropriate forms.

In the end, effects of smoking and its impact on various periodontal parameters have been summarized [Table 3].{Table 3}

 Conclusion



Smoking has a negative impact on the periodontal therapy. The prevalence and severity of periodontal disease in former smokers are between those of nonsmokers and current smokers. This implies that once the patient stops smoking, additional adverse effects are minimized. Cessation of smoking appears to allow the host to respond more like nonsmokers which provides basis for smoking cessation therapies. However, clinicians must be focused in their assessment of periodontal tissues because of appearance of healthy and nonbleeding gingiva. Smoking patients should follow a strict cessation program before the surgical procedures are done.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1Arora A, Mahan RN, Mhatre S, Bajaj A, Gopinath PV, Arvind P. Comparative evaluation of effect of smoking on survival of dental implant. J Int Oral Health 2017;9:24-7
2Hayman L, Steffen MJ, Stevens J, Badger E, Tempro P, Fuller B, et al. Smoking and periodontal disease: Discrimination of antibody responses to pathogenic and commensal oral bacteria. Clin Exp Immunol 2011;164:118-26.
3Centers for Disease Control and Prevention Cigarette smoking among adults. MMWR 48:1217;1997.
4Tomar SL, Asma S. Smoking-attributable periodontitis in the United States: Findings from NHANES III. J Periodontol 2000;71:743-51.
5Johnson GK, Slach NA. Impact of tobacco use on periodontal status. J Dent Educ 2001;65:313-21.
6Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005;366:1809-20.
7Buduneli N, Larsson L, Biyikoglu B, Renaud DE, Bagaitkar J, Scott DA. Fatty acid profiles in smokers with chronic periodontitis. J Dent Res 2011;90:47-52.
8Soysa NS, Ellepola AN. The impact of cigarette/tobacco smoking on oral candidosis: An overview. Oral Dis 2005;11:268-73.
9Borojevic T. Smoking and periodontal disease. Mater Sociomed 2012;24:274-6.
10Kirschneck C, Maurer M, Wolf M, Reicheneder C, Proff P. Regular nicotine intake increased tooth movement velocity, osteoclastogenesis and orthodontically induced dental root resorptions in a rat model. Int J Oral Sci 2017;9:174-84.
11Zee KY. Smoking and periodontal disease. Aust Dent J 2009;54 Suppl 1:S44-50.
12Palmer RM, Wilson RF, Hasan AS, Scott DA. Mechanisms of action of environmental factors-tobacco smoking. J Clin Periodontol 2005;32 Suppl 6:180-95.
13Vandana LK, Sridhar A. Tobacco use and its effects on the periodontium and periodontal therapy. J Contemp Dental Pract 2008;9:97-107.
14Michael NG, Henry TH, Perry KR, Fermin CA. Carranza's Clinical Periodontology Tenth Edition 2010.
15Tymkiw KD, Thunell DH, Johnson GK, Joly S, Burnell KK, Cavanaugh JE, et al. Influence of smoking on gingival crevicular fluid cytokines in severe chronic periodontitis. J Clin Periodontol 2011;38:219-28.
16Bagaitkar J, Daep CA, Patel CK, Renaud DE, Demuth DR, Scott DA. Tobacco smoke augments Porphyromonas gingivalis-Streptococcus gordonii biofilm formation. PLoS One 2011;6:e27386.
17Hayman L, Steffen MJ, Stevens J. Smoking and periodontal disease: discrimination of antibody responses to pathogenic and commensal oral bacteria. Clin Exp Immunol. 2011;164:118-26.
18Seow WK, Thong YH, Nelson RD, MacFarlane GD, Herzberg MC. Nicotine-induced release of elastase and eicosanoids by human neutrophils. Inflammation 1994;18:119-27.
19MacFarlane GD, Herzberg MC, Wolff LF, Hardie NA. Refractory periodontitis associated with abnormal polymorphonuclear leukocyte phagocytosis and cigarette smoking. J Periodontol 1992;63:908-13.
20Tsujii M, Iijima H, Nishida T, Takehara T. Smoking and alimentary diseases. Nippon Rinsho 2013;71: 436-42.
21Xu Y, Li H, Bajrami B, Kwak H, Cao S, Liu P, et.al. Cigarette smoke (CS) and nicotine delay neutrophil spontaneous death via suppressing production of diphosphoinositol pentakisphosphate Proc Natl Acad Sci 2013;110:7726-31.
22Stead LF, Perera R, Bullen C, Mant D, Hartmann-Boyce J, Cahill K, Lancaster T. Nicotine replacement therapy for smoking cessation. Cochrane Database of Systematic Reviews 2012;11:1465-858.
23Harmey D, Griffin PR, Kenny PJ. Development of novel pharmacotherapeutics for tobacco dependence: Progress and future directions. Nicotine Tob Res 2012;14:1300-18.
24Hartmann-Boyce J, Cahill K, Hatsukami D, Cornuz J. Nicotine vaccines for smoking cessation. Cochrane Database Syst Rev 2012;8:CD007072.
25Poggi P, Rota MT, Boratto R. The volatile fraction of cigarette smoke induces alterations in the human gingival fibroblast cytoskeleton. J Periodontal Res 2002;37:230-5.
26Noble RC, Penny BB. Comparison of leukocyte count and function in smoking and non-smoking young men. Infect Immun 1975;12:550-5.
27Kenney EB, Kraal JH, Saxe SR, Jones J. The effect of cigarette smoke on human oral polymorphonuclear leukocytes. J Periodontal Res 1977;12:227-34.
28Nadler JL, Velasco JS, Horton R. Cigarette smoking inhibits prostacycline formation. Lancet 1983;1:1248-50.
29Lawrence WT, Murphy RC, Robson MC, Heggers JP. The detrimental effect of cigarette smoking on flap survival: An experimental study in the rat. Br J Plast Surg 1984;37:216-9.
30Bain CA, Moy PK. The association between the failure of dental implants and cigarette smoking. Int J Oral Maxillofac Implants 1993;8:609-15.
31Bain CA. Smoking and implant failure-Benefits of a smoking cessation protocol. Int J Oral Maxillofac Implants 1996;11:756-9.
32Vehemente VA, Chuang SK, Daher S, Muftu A, Dodson TB. Risk factors affecting dental implant survival. J Oral Implantol 2002;28:74-81.
33Gorman LM, Lambert PM, Morris HF, Ochi S, Winkler S. The effect of smoking on implant failure at second stage surgery. Implant Dent1994;3:165-8.
34Lambert PM, Morris HF, Ochi S. The influence of smoking on 3-year clinical success of osseointegrated dental implants. Ann Periodontol 2000;5:79-89.
35Moy PK, Medina D, Shetty V, Aghaloo TL. Dental implant failure rates and associated risk factors. Int J Oral Maxillofac Implants 2005;20:569-77.
36Bezerra Ferreira JD, Rodrigues JA, Piattelli A, Iezzi G, Gehrke SA, Shibli JA. The effect of cigarette smoking on early osseointegration of dental implants: A prospective controlled study. Clin Oral Implants Res 2016;27:1123-8.
37Galindo-Moreno P, Fauri M, Avila-Ortiz G, Fernández-Barbero JE, Cabrera-León A, Sánchez-Fernández E. Influence of alcohol and tobacco habits on peri-implant marginal bone loss: A prospective study. Clin Oral Implants Res 2005;16:579-86.
38Grunder U, Gaberthuel T, Boitel N, Imoberdorf M, Meyenberg K, Andreoni C, et al. Evaluating the clinical performance of the Osseotite implant: Defining prosthetic predictability. Compend Contin Educ Dent 1999;20:628-33, 636, 638-40.
39Olson JW, Shernoff AF, Tarlow JL, Colwell JA, Scheetz JP, Bingham SF. Dental endosseous implant assessments in a type 2 diabetic population: A prospective study. Int J Oral Maxillofac Implants 2000;15:811-8.
40Bain CA, Weng D, Meltzer A, Kholes SS, Stach RM. A meta-analysis evaluating the risk for implant failure in patients who smoke. Compend 2002;23:695-706.