Influence of Moderate Cigarette Smoking on the Peri-Implant Clinicoradiographic Inflammatory Parameters Around Cement- and Screw-Retained Dental Implants

In clinical implant dentistry and related research, choice of retention (cement vs screw retained) for prosthesis retention continues to be a debatable subject.^1,2  Traditional clinical and laboratory-based techniques are used to fabricate cement-retained restorations, which makes this form of retention less challenging than screw-retained implant restorations.¹  Moreover, occlusal contacts are easily stabilized using cement-retained restorations as occlusal screw-access holes are absent in this form of implant prosthesis retention.^3,4  In the study by Hameed et al,⁵  screw-retained implant prostheses demonstrated significantly greater loss of crestal bone compared with cement-retained implant prosthesis. On the contrary, according to Al Amri et al,²  the mode of prosthesis retention does not influence the peri-implant clinical (bleeding on probing [BoP] and probing depth [PrD]) and radiographic (crestal bone resorption [CBR]) inflammatory parameters. According to Alqutaibi,⁶  implant survival rates of screw- and cement-retained dental implants are comparable. Nevertheless, it has also been proposed that accumulation of residual cement particularly at the restoration margins is a causative factor in the initiation of peri-implant soft-tissue inflammation.^7,8  This is often observed in situations in which the restoration margins extend at least 3 mm subgingivally.⁷ 

Cigarette smoking is a risk factor for diseases, including lung cancer and cardiomyopathies.^9–11  Studies^12–14  have also shown that molecular inflammatory events mediated by chronic smoking jeopardize oral soft tissues and expose vulnerable patients to oral diseases including oral cancer and chronic periodontitis (CrP). Moreover, in vitro results have shown that cigarette smoke extracts exert a cytotoxic effects and compromise cell viability in gingival fibroblasts.¹⁵  Furthermore, smoking induces a state of oxidative stress in periodontal tissues, which, if left uncontrolled, leads to bone loss around natural teeth and dental implants.¹⁶  In the study by Twito and Sade,¹⁶  cigarette smoking has also been shown to increase inflammation in peri-implant gingival tissues and supporting crestal bone. Pimentel et al¹⁷  assessed the oral microbiome among cigarette smokers and nonsmokers. The results showed that there was an abundance of pathogenic microbes (including Fusobacterium and Tannerella species) in the peri-implant biofilm compared with nonsmokers, in which microbes (such as Capnocytophaga, Actinomyces, and Streptococcus species) associated with a healthy peri-implant status were abundant.¹⁷ 

To the author's knowledge, there are no long-term follow-up studies comparing the peri-implant soft-tissue status and crestal bone levels around cement- and screw-retained dental implants in moderate cigarette smokers. The null hypothesis proposed in the present study is that there is no difference in peri-implant BoP, PrD, or CBR around cement- and screw-retained dental implants in moderate cigarette smokers. Therefore, the aim of the present 5-year follow-up retrospective cohort study was to compare the soft-tissue inflammatory parameters (BoP and PrD) and CBR around cement- and screw-retained dental implants in moderate cigarette smokers and nonsmokers.

The present study was based on a retrospective cohort study design. In the present study, patients (smokers and nonsmokers) who underwent dental implant treatment using cement- and screw-retained dental implants were clinically and radiographically evaluated at 5-year follow-up.

Patients were recruited from the outpatient department of a local hospital. Electronic dental records were searched from the years 2012 to 2015 to identify individuals who had received dental implants and had reported themselves as either smokers or nonsmokers. An invitation letter that explained the purpose of the present study was posted to these patients and accompanied by a stamped return envelope. Individuals who agreed to volunteer were invited and scheduled for a clinical and radiographic evaluation accordingly.

Moderate cigarette smokers (individuals smoking 11 to 15 cigarettes daily),¹⁸  nonsmokers (individuals who reported not using any form of tobacco product), and patients who underwent dental implant therapy with cement- and screw-retained restorations were included. Dual- and heavy smokers, smokeless tobacco users, alcohol users, and patients with self-reported systemic diseases such as acquired immune deficiency syndrome/HIV, diabetes mellitus, renal/hepatic diseases, and cardiovascular diseases were excluded. Implants placed in grafted sites were not sought. Moreover, patients who reported having consumed probiotics, antibiotics, steroids, and nonsteroidal anti-inflammatory medications within the past 2 months were also excluded.

Dental implants from a standardized implant system were assessed in the present study (SLA Active implant system, Straumann). All implants were placed under local anesthesia by an oral surgeon. In summary, in all groups, full-thickness mucoperiosteal flaps were raised, and an osteotomy was performed at a drilling speed of 2000 revolutions per minute under copious irrigation. In all groups, the implants were placed at bone level using an insertion torque of 30–35 Ncm. Soft-tissue closure was performed using nonresorbable sutures (UNIFY 3/0 e-PTFE surgical sutures). Prosthetic loading (using either cement- or screw-retained restorations) was done 3 to 3.5 months after implant insertion.

Information related to age, gender, duration of cigarette smoking (pack-years), duration of implants in function, jaw location of implants, and oral hygiene (brushing and flossing) was collected using a questionnaire. This questionnaire was administered to all patients by a trained investigator (Kappa score 0.92). Patients' dental records were also assessed to determine the features of implants (dimensions, surface characteristics, timing of implant placement, and cement used for restoration) that were placed.

In this study, CBR was calculated as the perpendicular distance from 2 mm under the abutment-implant junction up to the alveolar crestal height. This calculation was done on digital bitewing radiographs, which were taken using the long-cone paralleling technique.¹⁹  A positioner (X-ray Holders, KerrHawe.SA, Bioggio, Switzerland) was positioned on the 30.5- × 40.5-mm film (Kodak-Ultraspeed size-II Dental-Film, Kodak) parallel to the long axis of the implant and right-angled to the X-ray cone.¹⁹  The radiographs were also assessed for evidence of excess cement accumulation in the subgingival region. This assessment was done by the principal investigator (M.A.; Kappa score 0.9) who had an intraexaminer score of 0.92. The author (M.A.; Kappa score 0.9) measured the BoP and PrD around implants in all groups. The peri-implant sites (3 buccal and 3 palatal/lingual) were gently probed, and if the site exhibited bleeding, then it was recorded. The BoP was recorded as a percentage of sites per implant that bled on probing using the formula: (sites that bled/6 sites) × 100. The PrD was measured in millimeters using a plastic and graded probe.

A software package (SPSS, version 20) was used by an independent and experienced statistician to perform the statistical comparisons among the study groups. Group comparisons were performed using 1-way analysis of variance and Mann-Whitney U tests. For multiple comparisons, the Bonferroni post hoc adjustment test was carried out. Probability values (P values) less than .05 were considered significant. The sample size was estimated based on the results of a pilot investigation. It was estimated that inclusion of at least 24 smokers and nonsmokers with cement- and screw-retained dental implants would be needed to give the study a power of 90% with an alpha error of 5%.

Participation was completely voluntary, and all individuals reserved the right to withdraw from the study without penalty. Individuals who agreed to participate in the present investigation were provided an information sheet and sign a written informed consent form.

In total, 96 male individuals were included. Forty-eight patients (25 smokers and 23 nonsmokers) had cement-retained dental implants, and 48 (24 smokers and 24 nonsmokers) had screw-retained dental implants. Smokers with cement- and screw-retained dental implants were smoking 1.1 and 1.2 packs daily, respectively. Patients with cement- and screw-retained implants had a smoking history of 17.3 and 18 pack-years, respectively. In smokers and nonsmokers, cement- and screw-retained implants were in function for comparable durations (5 to 6 years). All patients had 1 dental implant placed in the maxilla or mandible. In patients with cement-retained dental implants, 84% of smokers and 82.6% of nonsmokers reported brushing their teeth once daily. Among patients with screw-retained dental implants, 91.7% smokers and 83.3% nonsmokers reported brushing their teeth once daily. None of the individuals reported having ever used dental floss (Table 1).

The cement- and screw-retained implants were platform switched and had moderately rough surfaces. All implants were bone level and were located in the region of missing premolars or molars. The implants had diameters and lengths ranging between 4.1–4.8 mm and 11–14 mm. In cigarette smokers, the cement- and screw-retained implants were in function since 5.7 (5–6 years) and 5.5 (5–5.7 years), respectively. In nonsmokers, the cement- and screw-retained implants were functional since 5.5 (5.1–6 years) and 5.4 years (5.2–5.9 years), respectively (Table 1). All implants were placed by a trained and experienced operator (M.A.).

Among patients with cement and screw-retained dental implants, PrD (P < .05) and CBR (P < .05) were significantly higher among smokers than nonsmokers. The peri-implant sites that demonstrated BoP were statistically significantly higher among nonsmokers (P < .05) than smokers among patients with cement- and screw-retained dental implants. There was no statistically significant difference in peri-implant PrD and CBR among smokers with cement- and screw-retained dental implants. Among nonsmokers with cement- and screw-retained dental implants, there was no statistically significant difference in BoP, PrD, or CBR (Table 2).

The current cohort study was based on the null hypothesis that there is no difference in peri-implant inflammatory parameters with reference to the type of prosthetic retention (cement vs screw retention) in cigarette smokers and nonsmokers. In other words, we hypothesized that cigarette smoking enhances peri-implant clinical and radiographic inflammatory parameters regardless of whether the implant prosthesis is cement or screw retained. The results showed that peri-implant PrD and CBR were significantly higher among cigarette smokers than nonsmokers with cement- and screw-retained dental implants. In this context, the results presented in this study are in accordance with the proposed null hypothesis. Studies^20–23  have shown that proinflammatory cytokines such as interleukin-1beta and tumor necrosis factor–alpha are more often expressed in the peri-implant sulcular fluid of smokers than nonsmokers. These cytokines enhance gingival inflammation and accelerate osteoclastic activity, which, if left uncontrolled, leads to peri-implant mucositis and peri-implantitis.^20–23  Moreover, habitual smoking augments a state of oxidative stress in the gingival tissues and enhances the formation and accumulation of advanced glycation end products (AGE) in oral fluids and gingival tissues. In a recent study, Akram et al²⁴  compared the levels of AGE in the gingival crevicular fluid (GCF) samples collected from patients with and without CrP. The results showed that AGE were more often expressed in the GCF of patients with than without CrP. The author applauds the study by Akram and coworkers²⁴  and hypothesizes that cigarette smoking enhances the expression of AGE in the peri-implant sulcular fluid, thereby augmenting soft-tissue inflammation and accelerating CBR in cigarette smokers than nonsmokers regardless of the mode of prosthetic retention used.

Subgingival accumulation of excess cement particularly at the implant-prosthesis junction may initiate peri-implant diseases (PiD) because of the difficulty in cleaning the region and excess plaque accumulation.⁷  In the present study, there was no radiographic evidence of excess cement accumulation in the subgingival region. One explanation for this is that all implants were placed by trained and experienced clinicians. In case there was excess cement accumulation in the subgingival region in cement-retained implant prosthesis, then PrD and CBR would be expected to higher among smokers with cement- than screw-retained dental implants. However, since bitewing radiographs are 2-dimensional images, the likelihood of excess cement accumulation in the lingual/palatal walls of the implant that are most likely shadowed by implant surfaces cannot be ignored. Further studies are needed in this regard. In the present study, more than 80% of participants were brushing their teeth once daily, and none reported having ever used dental floss. In this regard, the contribution of poor oral hygiene toward the initiation and progression of PiD should be considered. This result also suggests that health education and oral health counseling play a role in the maintenance of oral and peri-implant tissue health.

There are a number of limitations associated with the present study. First, it is pertinent to mention that the present study was performed in self-reported cigarette smokers. It is well-known that assessment of cotinine levels in fluids such as whole saliva is a more reliable method for determining the smoking status of an individual.^25,26  It is therefore likely that the whole salivary cotinine levels were significantly higher among the cigarette smokers than nonsmokers included in the present investigation. Second, the present study was performed exclusively in cigarette smokers. The primary reason for this is that cigarettes are the most common form in which tobacco is smoked.²⁷  However, other forms in which tobacco is smoked include cigars, pipes, and waterpipes (also known as hubble-bubble, narghile, or shisha). Studies^28–30  have shown that waterpipe users are as susceptible to PiD including peri-implantitis as cigarette smokers are. This suggests that PrD and CBR are higher around cement- and screw-retained implants placed in waterpipe users than in nonsmokers. It is also anticipated that cement- and screw-retained implants placed in waterpipe users and cigarette smokers are comparable in terms of progression of PiD. Another limitation is that a regression analysis after controlling for potential confounders such as age, gender, and smoking classification (mild, moderate, or heavy smoking) was not performed. One explanation for this is that all participants were male, and there was no statistically significant difference in the age of participants in the study groups. Moreover, on average, all participants were moderate smokers. Furthermore, at least 80% of the implants were located in the posterior mandible. Because bone density varies between the maxilla and the mandible, with the former being composed of dense bone,³¹  it is hypothesized that CBR is higher around cement- and screw-retained implants placed in the maxilla than in the mandible. Furthermore, systemic diseases such as a state of hyperglycemia (often manifested in diabetic and prediabetic patients) is also a risk factor for PiD. It has been reported that a state of persistent hyperglycemia increases the formation and accumulation of AGE in the gingival tissues of patients with poorly controlled diabetes.³²  This in turn compromises healing³²  and may result in loss of osteointegration regardless of the mode of implant prosthesis retention. It is therefore recommended that tobacco smokers and patients with a compromised systemic health status should be educated about the detrimental effects of smoking and immunosuppression on overall health. Furthermore, oral hygiene measures should be reinforced particularly among vulnerable patient groups, such as tobacco smokers. Such initiatives may help improve the oral health, success, and survival of dental implants and the overall quality of life of susceptible individuals. Additional studies are needed to investigate the stated speculations.

Cigarette smoking increases peri-implant soft-tissue inflammation as well as loss of crestal bone, and this relationship is independent of the type of implant retention protocol used.

The author thanks Mr Joanthan Förstrom, Statistical-solutions LLC, Fjardundrgatan 1441, Enkoping, Sweden, for performing the statistical analysis and Mr Gregory D'Silva from the Department of Medical Statistics, Kaymee Medical Center, Kuala Lampur Malaysia, for his kind assistance with statistical analysis.

The author declares that there is no conflict of interest and there was no external source of funding for the present study.