Abstract

Smoking has adverse effects on peri-implant bone healing and can cause bone loss around successfully integrated implants placed on type IV bone. This study evaluated the influence of implant surface topography of microimplants retrieved from posterior maxilla of smokers after 2 months of unloaded healing. Seven partially edentulous patients received 2 microimplants (machined and sandblasted acid-etched surface) each during conventional implant surgery. Histometric evaluation showed that the mean bone to implant contact was 10.40 ± 14.16% and 22.19 ± 14.68% to machined and sandblasted acid-etched surfaces, respectively (P < .001). These data suggest that the sandblasted acid-etched surface presented better results than the machined surface after a short healing time in smokers.

Introduction

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.35 In addition, these studies have shown firmer dental implant bone fixation with rough surfaces than with machined implants.3,4,68 Consequently, it has been suggested that rough surface implants can be loaded at an earlier period than machined surfaces.913 

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.

Material and Methods

Subject selection

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.

Microimplants and surface preparation

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.

Figure 1

(a) Scanning electron microscopy of the microimplant evaluate and atomic force microscopy of the implant surface topography. (b) Machined implant surface. (c) Sandblasted acid-etched surface.

Figure 1

(a) Scanning electron microscopy of the microimplant evaluate and atomic force microscopy of the implant surface topography. (b) Machined implant surface. (c) Sandblasted acid-etched surface.

Implant surgery

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.

Specimen processing

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.

Results

Clinical observations

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.

Histologic and histometric results

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.

Figures 2–5

Figure 2. Bone tissue is scarce around sandblasted acid-etched surface (Acid fuchsin and toluidine blue, original magnification ×16). Figure 3. Ground section of sandblasted acid-etched surface presenting osteoblasts connected (arrows) to newly formed bone tissue (NB) and connective tissue (CT). (Acid fuchsin and toluidine blue, original magnification ×100). Figure 4. Immature bone is present around the machined implant. The peri-implant bone presents early stages of maturation (NB) in contact with the pristine bone (arrows, OB). However, the NB stop before contact with the implant surface (I), suggesting indirect osteogenesis (Acid fuchsin and toluidine blue, original magnification ×40). Figure 5. Histologic ground section of machined surface presenting apposition of connective tissue (CT) between the newly formed bone (NB) in the apical area of the microimplant (Acid fuchsin and toluidine blue, original magnification ×40).

Figures 2–5

Figure 2. Bone tissue is scarce around sandblasted acid-etched surface (Acid fuchsin and toluidine blue, original magnification ×16). Figure 3. Ground section of sandblasted acid-etched surface presenting osteoblasts connected (arrows) to newly formed bone tissue (NB) and connective tissue (CT). (Acid fuchsin and toluidine blue, original magnification ×100). Figure 4. Immature bone is present around the machined implant. The peri-implant bone presents early stages of maturation (NB) in contact with the pristine bone (arrows, OB). However, the NB stop before contact with the implant surface (I), suggesting indirect osteogenesis (Acid fuchsin and toluidine blue, original magnification ×40). Figure 5. Histologic ground section of machined surface presenting apposition of connective tissue (CT) between the newly formed bone (NB) in the apical area of the microimplant (Acid fuchsin and toluidine blue, original magnification ×40).

Discussion

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.15,2022 

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.

Abbreviations

     
  • BD

    bone area

  •  
  • BIC

    bone to implant contact

  •  
  • ROI

    reactive oxygen species

Acknowledgments

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

References

References
1
Albrektsson
,
T.
,
P. I.
Branemark
,
H. A.
Hansson
, and
J.
Lindstrom
.
Osseointegrated titanium implants.
Acta Orthopaedica Scandinavica
1981
.
52
:
155
170
.
2
Abrahamsson
,
I.
,
T.
Berglundh
,
E.
Linder
,
N. P.
Lang
, and
J.
Lindhe
.
Early bone formation adjacent to rough and turned endosseous implant surfaces. An experimental study in the dog.
Clin Oral Implants Res
2004
.
15
:
381
392
.
3
Buser
,
D.
,
R. K.
Schenk
,
S.
Steinemann
,
J. P.
Fiorellini
,
C. H.
Fox
, and
H.
Stich
.
Influence of surface characteristics on bone integration of titanium implants. A histomorphometric study in miniature pigs.
J Biomed Mater Res
1991
.
25
:
889
902
.
4
Buser
,
D.
,
T.
Nydegger
,
H. P.
Hirt
,
D. L.
Cochran
, and
L. P.
Nolte
.
Removal torques values of titanium implants in the maxilla of miniature pigs.
Int J Oral Maxillofac Implants
1998
.
13
:
611
619
.
5
Shalabi
,
M. M.
,
J. G.
Wolke
, and
J. A.
Jansen
.
The effects of implant surface roughness and surgical technique on implant fixation in an in vitro model.
Clin Oral Implant Res
2006
.
17
:
172
178
.
doi:10.1111/j.1600-0501.2005.01202.x.
6
Wennerberg
,
A.
,
T.
Albrektsson
,
B.
Andersson
, and
J. J.
Kroll
.
A histomorphometrical and removal torque study of screw-shaped titanium implants with three different surface topographies.
Clin Oral Implants Res
1995
.
6
:
24
30
.
7
Wennerberg
,
A.
,
T.
Albrektsson
,
C. B.
Johanson
, and
B.
Andersson
.
Experimental study of turned and grit blasted screw-shaped implants with special emphasis on effects of blasting material and surface topography.
Biomaterials
1996
.
17
:
15
22
.
8
Hallgren
,
C.
,
T.
Sawase
,
U.
Ortengren
, and
A.
Wennerberg
.
Histomorphometric and mechanical evaluation of the bone-tissue response to implants prepared with different orientation of surface topography.
Clin Implant Dent Relat Res
2001
.
3
:
194
203
.
9
Shibli
,
J. A.
,
S.
Grassi
, and
L. C.
de Figueiredo
.
Influence of implant surface topography on early osseointegration: a histological study in human jaws.
J Biomed Mater Res B Appl Biomater
2007
.
80
:
377
385
.
10
Shibli
,
J. A.
,
S.
Grassi
,
L. C.
de Figueiredo
,
M.
Feres
,
G.
Iezzi
, and
A.
Piattelli
.
Human peri-implant bone response to turned and oxidized titanium implants inserted and retrieved after 2 months.
Implant Dent
2007
.
16
:
252
259
.
11
Shibli
,
J. A.
,
M.
Feres
,
L. C.
de Figueiredo
,
G.
Iezzi
, and
A.
Piattelli
.
Histological comparison of bone to implant contact in two types of dental implant surfaces: a single case study.
J Contemp Dent Pract
2007
.
8
:
29
36
.
12
Grassi
,
S.
,
A.
Piattelli
,
L. C.
de Figueiredo
, et al
.
Histologic evaluation of early human bone response to different implant surfaces.
J Periodontol
2006
.
77
:
1736
1743
.
13
Grassi
,
S.
,
A.
Piattelli
,
D.
Ferari
, et al
.
Histologic evaluation of human bone integration on machined and sandblasted acid-etched titanium surfaces in type IV bone.
J Oral Implantol
2007
.
33
:
8
12
.
14
Cesar-Neto
,
J. B.
,
P. M.
Duarte
,
E. A.
Sallum
,
D.
Barbieri
,
H.
Moreno
Jr
, and
F. H.
Nociti
Jr
.
A comparative study on the effect of nicotine administration and cigarette smoke inhalation on bone healing around titanium implants.
J Periodontol
2003
.
74
:
1454
1459
.
15
Nociti
Jr,
F. H.
,
N. J.
Cesar
,
M. D.
Carvalho
, and
E. A.
Sallum
.
Bone density around titanium implants may be influenced by intermittent cigarette smoke inhalation: a histometric study in rats.
Int J Oral Maxillofac Implants
2002
.
17
:
347
352
.
16
Bolin
,
A.
,
G.
Eklund
,
L.
Frithiof
, and
S.
Lavstedt
.
The effect of changed smoking habits on marginal alveolar bone loss. A longitudinal study.
Swed Dent J
1993
.
17
:
211
216
.
17
Feloutzis
,
A.
,
N. P.
Lang
,
M. S.
Tonetti
, et al
.
IL-1 gene polymorphism and smoking as risk factors for peri-implant bone loss in a well-maintained population.
Clin Oral Implants Res
2003
.
14
:
10
17
.
18
Bain
,
C. A.
Implant installation in the smoking patient.
Periodontol 2000
2003
.
33
:
185
193
.
19
Shibli
,
J. A.
,
S.
Grassi
,
A.
Piattelli
, et al
.
Histomorphometric evaluation of bioceramic molecular impregnated and dual acid etched implant surfaces in the human posterior maxilla.
Clin Implant Dent Relat Res
2009
.
(in press). doi:10.0000/j.1708-8208.2009.00174.x.
20
Saldanha
,
J. B.
,
S. P.
Pimentel
,
M. Z.
Casati
,
A. W.
Sallum
,
E. A.
Sallum
, and
F. H.
Nociti
.
Histologic evaluation of the effect of nicotine administration on bone regeneration. A study in dogs.
Braz Oral Res
2004
.
18
:
345
349
.
21
Stefani
,
C. M.
,
F.
Nogueira
,
E. A.
Sallum
,
T. S.
de
,
A. W.
Sallum
, and
F. H.
Nociti
Jr
.
Influence of nicotine administration on different implant surfaces: a histometric study in rabbits.
J Periodontol
2002
.
73
:
206
212
.
22
Cesar-Neto
,
J. B.
,
B. B.
Benatti
,
E. A.
Sallum
,
A. W.
Sallum
, and
F. H.
Nociti
Jr
.
Bone filling around titanium implants may benefit from smoking cessation: a histologic study in rats.
J Periodontol
2005
.
76
:
1476
1481
.
23
Casper
,
R. F.
,
M.
Quesne
,
I. M.
Rogers
, et al
.
Resveratrol has antagonist activity on the aryl hydrocarbon receptor: implications for prevention of dioxin toxicity.
Mol Pharmacol
1999
.
56
:
784
790
.
24
Ramp
,
W. K.
,
L. G.
Lenz
, and
R. J.
Galvin
.
Nicotine inhibits collagen synthesis and alkaline phosphatase activity, but stimulates DNA synthesis in osteoblast-like cells.
Proc Soc Exp Biol Med
1991
.
197
:
36
43
.
25
Duthie
,
G. G.
,
J. R.
Arthur
, and
W. P.
James
.
Effects of smoking and vitamin E on blood antioxidant status.
Am J Clin Nutr
1991
.
53
(
suppl
):
1061S
1063S
.
26
Garrett
,
I. R.
,
B. F.
Boyce
,
R. O.
Oreffo
,
L.
Bonewald
,
J.
Poser
, and
G. R.
Mundy
.
Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo.
J Clin Invest
1990
.
85
:
632
639
.
27
Ries
,
W. L.
,
L. L.
Key
Jr
, and
R. M.
Rodriguiz
.
Nitroblue tetrazolium reduction and bone resorption by osteoclasts in vitro inhibited by a manganese-based superoxide dismutase mimic.
J Bone Miner Res
1992
.
7
:
931
939
.
28
Den Braber
,
E. T.
,
J. E.
De Ruijter
,
H. T. J.
Smits
,
L. A.
Ginsel
,
A. F.
Von Recum
, and
J. A.
Jansen
.
Effect of parallel surface microgrooves and surface energy on cell growth.
J Biomed Mater Res
1995
.
29
:
511
518
.
29
Lumbikanonda
,
N.
and
R.
Sammons
.
Bone cell attachment to dental implants of different surface characteristics.
Int J Oral Maxillofac Implants
2001
.
16
:
627
636
.
30
Yan
,
W. Q.
,
T.
Nakamura
,
M.
Kobayashi
,
H. M.
Kim
,
F.
Miyaji
, and
T.
Kokubo
.
Bonding of chemically treated titanium implants to bone.
J Biomed Mater Res
1997
.
37
:
267
275
.

Author notes

1

Oral Implantology Clinic, Guarulhos University, Guarulhos, São Paulo, Brazil.

2

Department of Periodontology, Dental Research Division, Guarulhos University, Guarulhos, São Paulo, Brazil.

3

University of Chieti-Pescara, Chieti, Italy.