Impact of Smoking on Human Bone Apposition at Different Dental Implant Surfaces: A Histologic Study in Type IV Bone

Earlier studies1,2 have suggested that implant surface topography was the only parameter that significantly affected bone to implant contact (BIC) and interface shear strength. These findings were later confirmed by studies with animals, which indicated that a certain degree of surface roughness favored BIC, as assessed by the removal torque test.3–5 In addition, these studies have shown firmer dental implant bone fixation with rough surfaces than with machined implants.3,4,6–8 Consequently, it has been suggested that rough surface implants can be loaded at an earlier period than machined surfaces.9–13 

However, systemic conditions such as smoking can influence bone healing14,15 and can increase the progression of bone loss.16,17 It has been suggested that smokers suffer detrimental effects around successfully integrated implants inserted on type IV bone. On the other hand, specific factors such as microstructure may also enhance the bone apposition mainly in smokers.18 At present there is little information on human bone tissue response to sandblasted acid-etched surface during early osseointegration in smokers.

The aim of this study was to evaluate the impact of implant surface topography in the BIC percentage in microimplants retrieved from posterior maxilla (type IV bone) of smokers.

The study included 7 partially edentulous smokers (3 women, 4 men) with a mean age of 63 years (range, 37–68 years) who were referred to the Oral Implantology Clinic, Guarulhos University, Brazil, for oral rehabilitation with implant-supported restoration. Smokers were included based on smoking habits (>10 cigarettes a day for at least 10 years). Exclusion criteria included nonsmokers and former smokers, pregnancy, nursing, and any systemic conditions that could affect bone healing, such as osteoporosis and blood disorders. The local Ethics Committee for Human Clinical Trials approved the study protocol.

Fourteen screw-shaped microimplants, 2.2 mm in diameter and 4 mm long, made of grade-4 titanium (AS Technology Titanium-FIX, São José dos Campos, São Paulo, Brazil) were prepared with 2 surface topographies: machined and sandblasted acid-etched surfaces (Figure 1). The microimplants with sandblasted acid-etched surface were blasted with 100 µm Al₃O₂ particles. After sandblasting, the specimens were ultrasonically cleaned with an alkaline solution, washed in distilled water, and pickled with HNO₃.

All microimplants were placed in the posterior maxilla during the surgical procedures for conventional dental implant placement as previously reported.9,12,19 After incision, mucoperiosteal flaps were raised, and the conventional implants were placed. Next, the 2 microimplants—1 with a machined and 1 with an sandblasted acid-etched surface—were placed mostly in the upper molar region, that is, posterior to the most distal conventional implant. A coin determined the position of the sandblasted acid-etched surface (in an anterior or posterior position to the last conventional implant). The microimplant recipient sites were prepared with a 1.8 mm diameter twist drill, and implants were inserted with a screwdriver. All drilling and microimplant placement procedures were completed under profuse irrigation with sterile saline. If the microimplant showed low primary stability, a backup surgical site was prepared. The flaps were sutured with single interrupted sutures to submerge all the dental implants, including the microimplants. Clindamicin was given twice a day for a week, to avoid postsurgical infection; pain was controlled with acetaminophen and the sutures were removed after 10 days.

A total of 14 microimplants (7 controls and 7 tests) were placed in 7 maxillae. After 2 months of unloaded healing, the microimplants were removed, using an internal 3.25 mm wide trephine, and the microimplants, together with surrounding bone tissues, were rinsed in sterile saline solution and fixed by immersion in 4% neutral formalin.

To process the microimplants and surrounding bone tissues to obtain thin ground sections with the Precise 1 Automated System (Assing, Rome, Italy), the specimens were dehydrated in an ascending series of alcohol rinses and embedded in a glycol methacrylate resin (Technovit 7200 VLC, Kulzer, Wehrheim, Germany). After polymerization, the specimens were sectioned longitudinally along the major implant axis with a high-precision diamond disk at about 150 µm, and ground down to about 30 µm. Two slides were obtained for each implant. The slides were stained with basic fuchsin and toluidine blue. Histomorphometry of BIC percentage, as well as the bone area within the limits of the implant threads, were performed with a light microscope (Laborlux S, Leitz, Wetzlar, Germany) connected to a high-resolution video camera (3CCD, JVC KY-F55B, Milan, Italy) and interfaced with a monitor and personal computer (Intel Pentium III 1200 MMX, Santa Clara, Calif). This optical system was associated with a digitizing pad (Matrix Vision GmbH, Milan, Italy) and a histometry software package with image-capturing capabilities (Image-Pro Plus 4.5, Media Cybernetics, Immagini & Computer Snc, Milan, Italy).

The BIC and the amount of bone area (BD) within the threads (measured, from the lowest point of the microimplant head to the last apical thread) were calculated and expressed as percentage of BIC and percentage of BD, respectively. Mean and standard deviation were calculated. The Mann-Whitney test was used for comparison between the different implant surface topographies. Significance test was 2-tailed and conducted at a 5% significant level.

Before retrieval, 2 machined microimplants, were mobile at the time of retrieval. The 2 unstable microimplants were included in the statistical evaluation as 0 values.

The pristine bone was D4. The retrieved microimplants depicted healthy peri-implant bone. Osteocytes were presented in their lacunae, although areas of woven bone could be distinguished. The newly formed peri-implant bone exhibited early stages of maturation, mainly on the sandblasted acid-etched surface (Figure 2). In this area it was possible to observe that many osteoblasts were present inside the gap depositing osteoid matrix in the apicocoronal direction. Some slides presented osteoblasts connected to newly formed peri-implant bone, showing ongoing bone formation, and minor apposition of new peri-implant bone could be found, specifically inside the implant threads of the sandblasted acid-etched surface (Figure 3). Gaps and fibrous tissue are presented mainly around machined surface specimens (Figures 4 and 5). The connective tissue was loose with scattered inflammatory cells. Both histometric variables were significantly higher (P < .001) in the sandblasted acid-etched surface group. Histometric evaluation showed that mean BIC was 10.40 ± 14.16 and 22.19 ± 14.68 to machined and sandblasted-acid etched surfaces, respectively. The BD ranged between 17.23 ± 10.32 for machined and 24.12 ± 11.23 for sandblasted surface.

The present study evaluated the influence of implant surface topography on early bone healing of retrieved implants from smokes. The histometric data showed that the sandblasted acid-etched surface topography presented better histometric results in smokers.

Cigarette smoking is related to severity and progression of periodontal diseases, impaired bone healing, and higher rate of implant failure. Previous animal studies have shown that smoking interferes negatively with osseointegration and regenerative procedures.15,20–22 

Peri-implant bone healing is a complex process, involving a cascade of synthesis and activation of matrix proteins, growth factors, cytokines, and angiogenic stimulators that coordinate the restoration of bone mechanical stability at the peri-implant interface. Despite the knowledge that cigarette smoking is a risk factor for implant loss, the mechanism responsible for the adverse effects of cigarette smoke on peri-implant bone is currently under research. One difficulty lies in fact that cigarette smoke is composed of more than 4000 different chemicals.23 For example, the sequential expression of type I collagen, alkaline phosphatase, and osteocalcin, besides the deposition of calcium, have been affected by cigarette smoking, mainly by the nicotine.24 In addition, smoking is associated with an increased concentration of reactive oxygen species (ROIs) and reduced levels of vitamins.25 Several studies have suggested that ROIs may be increased in the bone resorption process.26,27 

Although cigarette smoking has a detrimental effect on BIC, the data from this study agree with the recent experimental studies9,12,13 where surface topography increased BIC in nonsmokers, at least under unloaded conditions. The implant surface topography of sandblasted acid-etched surfaces entails mechanical restrictions to the spread and locomotion of the cells involved in bone healing.28,29 

In turn, each of these events is affected by physicochemical interaction between the molecules and cells in the surrounding area30 and cigarette smoking affects all of these processes. However, the implant surface topography properties could enhance the organization of the cascade of events in the peri-implant area, increasing the newly formed bone and, consequently, the long-term success of the implant supported restoration.

It must be pointed out that the implant design used in the present research has only research purpose and does not allow direct comparisons with previous clinical trials; however, the present data may suggest that the use of roughness surfaces at micrometer level can enhance the osseointegration, mainly in type IV bone. Within the limits of this study, it can be assumed that implant surface topography may positively influence the osseointegration around implants placed in type IV bone of smokers. However, further studies carried out with nonsmokers could present a clear influence of smoking on bone implant healing.

BD

bone area

BIC

bone to implant contact

ROI

reactive oxygen species

The authors would like to thank Titanium-FIX, São Paulo, Brazil, for supplying the experimental implants.