This study evaluated the clinical, radiographic, and histologic responses of tissues surrounding implants loaded with a heavy force of 500g for 20 weeks after a 1-week healing period. Unilateral mandibular and maxillary alveolar ridges in the premolar areas of a male dog and the bilateral mandibular alveolar ridges of a female dog were chosen for implant placement. The control implants (1 in the maxilla, 3 in the mandible) were placed in these quadrants after a 12-week healing period following extraction. The test implants (1 in the maxilla, 3 in the mandible) were implanted in the same quadrants after a 4-month osseointegration period of the control implants. Abutments were attached to the control and test implants after a 1-week healing period for the test implants. Superelastic nickel-titanium coil springs, producing a force of 500g (≈5 N), were activated between control and test implants for 20 weeks. Light microscopic assessment revealed that all implants were well integrated with the bone. Histologic analysis showed no definitive differences between test and control implants in the corticalization of bone trabeculae. The mean bone-implant contact values of the control implants for compression and tension sides were 55.99% and 64.04%, respectively. In the test implants, the bone-implant contact value was 57.27% for the compression side and 62.96% for the tension side. Potential clinical applications of these radiologic and histologic results include the possibility of minimizing the healing duration, even for high orthodontic forces, and the possibility of postorthodontic use of these implants as abutments for supporting prosthetic reconstruction.

Introduction

Anchorage is resistance to the forces exerted by other teeth or devices. Dental implants are used for orthodontic anchorage; they can withstand orthodontic loading and provide excellent sources of anchorage.1 Indications for using dental implants for orthodontic anchorage include the following: to correct intruded/extruded teeth; to close edentulous spaces; to reposition malpositioned teeth; to reinforce anchorage; and to correct partial edentulism, undesirable occlusion, and orthopedic movement.2 

Stability and rigidity are the most important factors in the durability of implants in resisting reaction forces.2 Numerous clinical36 and animal722 studies have demonstrated the success of dental implants for orthodontic anchorage purposes. In these studies, the force levels ranged from 60 to 600g of distalizing or pulling forces in implant-implant or implant-tooth, and the healing time before loading varied from 4 to 25 weeks. Observation periods ranged from 1 to 39 months.

However, most of these studies have in common long healing periods following implant insertion and before orthodontic loading. Few animal15,23 and human2426 studies have investigated osseous changes after early or immediate loading.

The aim of the present study was to evaluate the bone tissue response of early loaded (at 1 week) and osseointegrated implants used as orthodontic anchorage units after a lateral heavy force application of 500g for 20 weeks.

Materials and Methods

Two adult Turkish Sheepdogs (2 years old; 1 male and 1 female) weighing 20 to 25 kg were used as subjects in this study. Unilateral mandibular and maxillary alveolar ridges in the premolar areas of the male dog and bilateral mandibular alveolar ridges of the female dog were chosen for implantation. To provide an edentulous alveolar ridge for implantation, all of the premolars were extracted, and the alveolar ridges were left to heal for 12 weeks. During the extractions, the dogs were anesthetized with intramuscular injections of ketamine HCl (Ketalar, Parke Davis, Istanbul, Turkey) at 10 mg/kg of body weight, and xylazine HCl (Rompun, Bayer, Istanbul, Turkey) at 2.2 mg/kg of body weight. Treatment of the experimental animals had been approved by the Turkish Ministry of Health's Animal Research and Ethics Committee.

The implants used in this study were tapered fixtures with self-tapping screws and microtextured surface (SPMB 8, Zimmer, Carlsbad, Calif). The intraosseous portion of the implants features a medium-rough, microtextured surface (MTX) created by blasting with soluble hydroxyapatite, followed by a mild, nonetching wash to remove manufacturing debris. The implants, with an endosseous length of 8 mm and a diameter of 3.7 mm, were placed in the healed extraction sites in the maxilla and mandible.

The control implants were left to heal for 4 months. After this osseointegration period, the test implants were placed in the same quadrant. Postoperatively, the animals received ampicillin and sulbactam at doses of 1000 mg and 500 mg, respectively, per day (Duocid, Pfizer, Istanbul, Turkey). Dental hygiene was maintained by brushing and rinsing the dogs' teeth once daily with 0.2% chlorhexidine gluconate solution.

After a 1-week healing period, abutments were attached to the test (1 in the maxilla, 3 in the mandibles) and control group implants (1 in the maxilla, 3 in the mandibles). Two medium and 1 heavy superelastic nickel-titanium (Ni-Ti) coil springs (No. 10-000-01 and 10-000-02, GAC International, Bohemia, NY) were used to produce a continuous force of 500g (≈5 N) for 20 weeks. The superelastic Ni-Ti coil springs were ligatured to the abutments of the test and control implants. The direction of force was perpendicular to the long axis of the implants. The dogs were put on a soft-food diet for the duration of the experiment to ensure long-term functioning of the coil springs.

Before the application of force, periapical radiographs were taken with the parallel technique to examine the bone tissue around implants. In addition, to assess whether or not the implants were dislocated during the force application period, casts were obtained to determine the implant-canine and implant-neighboring molar distances for each subject. After the application of force for 20 weeks, radiographs were taken again, and casts were obtained. The distances between implants and neighboring teeth were measured with digital calipers. Moreover, probing depth measurements were recorded for the mesial and distal aspects of the control and test implants at the start and termination of the force application period.

The animals were put down at the end of the experiment. Subsequently, the alveolar processes containing the implants were dissected out, and the implants and surrounding tissues were stored in a 10% neutral-buffered formalin solution. Histologic specimens prepared in the sagittal plane were infiltrated with remacryl resin from a starting solution of 50% ethanol and 50% resin, and subsequently 100% resin. This procedure included 8 steps, with each step lasting 24 hours. Photopolymerization was achieved by 48-hour exposure to blue light (280–320 nm). After polymerization, the blocks were ground to remove excess resin and to expose the implant, and then were glued to plastic slides with methacrylate-based glue.

A Micromet high-speed rotating blade microtome (Remet, Bologna, Italy) was used to produce 250-µm-thick sections from the block. Each section was then ground down to approximately 40 µm with an LS-2 grinding machine (Remet) equipped with waterproof grinding paper. After the grinding procedure, each section was polished with 2400 silicon carbide polishing paper (SIC-Paper, Struers A/S, Copenhagen, Denmark) and 3-µm polishing cream (Tremillimetri, Brook Italia, Settimo Milanese, Milan, Italy). Toluidine-blue stain was used to determine the different ages and remodeling patterns of bone, and basic fuchsin was used to distinguish the fibrous tissue and to enhance contrast.

Histomorphometric analysis was performed by digitizing the images from the described microscope via a JVC TK-C1380 color video camera (JVC Victor Company, Tokyo, Japan) and a frame grabber. Images, including the entire implant surface, were obtained with a ×10 objective lens and were analyzed with IAS 2000 image analysis software (Delta Sistemi, Rome, Italy). For each implant, the 2 most centralized sections were analyzed. The percentage of bone-implant contact (BIC) was calculated by comparing it with the total length of the implant interface. The BIC, which is the linear surface of the implant directly contacted by the bone matrix, is expressed as a percentage of the total implant surface.

Results

Clinical findings

Despite daily brushing and rinsing with 0.2% chlorhexidine gluconate solution, the 2 dogs suffered from slight gingivitis and mucositis around the test and control implants. No mobility or loss of implants was observed, and the pocket depths of the implants were constant, except for 1 implant that was subjected to functional forces because of premature contact with the lower teeth. This control implant and the corresponding test implant were deleted from the study. The mean pocket depth changes are shown in Table 1. After orthodontic loading of the implants, their mean dislocation was 0.03 ± 0.01 mm; for the control implants, it was 0.02 ± 0.01 mm. However, these dislocations were not statistically significant (P > .05).

Table 1

Differences in pocket depth (mean ± SD) around implants before and after orthodontic force application

Differences in pocket depth (mean ± SD) around implants before and after orthodontic force application
Differences in pocket depth (mean ± SD) around implants before and after orthodontic force application

Radiologic analysis

Radiologic analysis showed bone tissue with a normal trabecular pattern. No obvious radiolucencies were seen around or underneath the implants in radiographic and tomographic analyses, except in 1 control implant that had been subjected to functional forces through premature contact with lower teeth (Figure 1). An increase in compact bone, characterized by increased radiopacity, was observed around the coronal region of both test and control implants.

Figure 1.

Radiograph of the alveolar bone around the implants. Maxillary control (*) and test implants (a) before and (b) after force application. Dislocation and bone loss of maxillary control (*) implant due to “excessive occlusal load.” Mandibular control and test implants (c) before and (d) after force application.

Figure 1.

Radiograph of the alveolar bone around the implants. Maxillary control (*) and test implants (a) before and (b) after force application. Dislocation and bone loss of maxillary control (*) implant due to “excessive occlusal load.” Mandibular control and test implants (c) before and (d) after force application.

Histologic analysis

Light microscopic assessments demonstrated that all implants were well integrated with the bone. Histologic assessment showed no definite differences concerning corticalization of bone trabeculae between test and control implants. A slight increase in bone density was seen at the pressure sides of both test and control implants, and induced bone apposition at the crestal areas of the compression sides compared with the tension sides was observed, although this difference was very slight.

The control implants (Figure 2) were fully immersed in the alveolar bone. Woven and composite bone healing was visible. Thinner, continuous bony trabeculae, which surrounded the implants, were mainly oriented perpendicular to the fixture surface on the compression side, where the density of bone was lower than on the tension side, where the bone was dense composite and had primary osteons. Periosteal and endosteal bone formation was evident as thin osteoid layers covering free bone tissue. The cutting-filling cones in the cortical bone showed internal remodeling. A thin bone layer surrounded the endosseous implant surface up to the apex. No significant differences were visible between the tension and compression sides.

Figure 2.

(a) Mandibular control implant: Continuous bony trabeculae surround all implant surfaces in the (b) coronal and (c) middle regions of the compression (*) side; dense composite bone with primary osteons is evident in the (d) coronal and (e) middle regions of the tension side.

Figure 2.

(a) Mandibular control implant: Continuous bony trabeculae surround all implant surfaces in the (b) coronal and (c) middle regions of the compression (*) side; dense composite bone with primary osteons is evident in the (d) coronal and (e) middle regions of the tension side.

In the test implants (Figure 3), the coronal part of the fixture was integrated into the crestal bone. The crestal bone surrounding the fixture in this region was composed of a dense cortical layer and a poor soft marrow cavity, which was more prominent on the compression sides. The cortical bone in the coronal area showed internal remodeling with cutting-filling cones. The inner portion of the bone surrounding the fixtures was similar to the inner portion of the medullary canal of long bones. The interface below the crest showed thicker trabeculae, whereas more apically, the trabeculae covering the fixtures became thinner. Corticalization of the bone was evident at the apex of the implant, where the BIC was also higher. The apical area was constituted mostly of dense bone. No significant differences were found between the pressure and tension surfaces of the test implants relative to bone quality and density (P > .05).

Figure 3.

(a) Mandibular test implant: Light bone resorption activity is evident in the (b) coronal area of the compression (*) side, but not in the (c) coronal area of the tension side. Few thin trabeculae are present in the (d) middle region of the compression (*) side and the (e) middle region of the tension side.

Figure 3.

(a) Mandibular test implant: Light bone resorption activity is evident in the (b) coronal area of the compression (*) side, but not in the (c) coronal area of the tension side. Few thin trabeculae are present in the (d) middle region of the compression (*) side and the (e) middle region of the tension side.

The percentages of osseointegration (BIC) and bone density (ie, bone volume [BV]) determined by histomorphometric analyses are shown in Tables 2 and 3. The percentages of BIC and BV showed no significant differences between tension and compression sides (P > .05). According to these observations, a stable bone-implant contact zone was maintained in both test and control implant groups throughout the force application period.

Table 2

Percentage of bone-implant contact at compression and tension areas of test and control implants

Percentage of bone-implant contact at compression and tension areas of test and control implants
Percentage of bone-implant contact at compression and tension areas of test and control implants
Table 3

Percentage of bone volume at compression and tension areas of test and control implants

Percentage of bone volume at compression and tension areas of test and control implants
Percentage of bone volume at compression and tension areas of test and control implants

Discussion

In the present study, the control group implants, with 1 exception, showed no clinical mobility, losses, or significant displacement throughout the force application period. This shows that the control implants remained stable and maintained direct bone anchorage during loading, which is in accordance with the findings of other animal studies,8,14,18,19 in which different force levels were applied, as well as human studies.6,22,27 One control implant showed mobility and dislocation during the 20-week observation period caused by “excessive occlusal load.” Isidor28 reported that 5 of 8 implants lost osseointegration, as determined radiographically and histologically, within 4.5 to 15.5 months after excessive occlusal loading.

One of the most important clinical findings of the present study was that the test implants showed no clinical mobility, losses, or significant displacement throughout the force application period. The unloaded healing period for test implants was 1 week after implant insertion. Limited animal15,23 and human2426 studies have also evaluated stabilization of implants after a short healing period. Majzoub et al15 reported no dislocation throughout the force application period, following a 2-week unloaded healing period. A histomorphometric study by Borsos et al25 demonstrated that a nonloaded healing period of 12 weeks did not lead to significant improvement in osseointegration compared with loading within 72 hours. Immediate loading of palatal implants for maximum anchorage did not increase the risk to patients or adversely affect treatment results.25 Immediate26 and early24 loaded palatal implants showed an initial decrease in their implant stability quotient (ISQ) values. However, Jackson et al26 reported that palatal orthodontic implants could be immediately loaded and successfully used for orthodontic purposes when primary stability was observed at the time of implant placement.

In the present study, mean pocket depth of the test group following orthodontic loading fell from 3.0 mm to 2.8 mm, while the control group's depth rose from 2.1 mm to 2.7 mm. The peri-implant gingiva consistently displayed signs of low-grade inflammation and temporarily bled slightly on probing. Turley et al,9 Smalley et al,10 Wehrbein and Diedrich,20 Wehrbein et al,12 Melsen and Lang,18 and Aldıkaçtı et al19 reported similar findings. In addition, the current study revealed no visual differences between control and test implants.

Radiographic and tomographic images of the test and control group implants revealed a normal bone pattern around the implants. No radiolucency was obvious around the anchorage units. In all implants, the level of bone was above the highest groove of the implants. Radiographic evaluation from the current study supports the findings of Turley et al,9 Roberts et al,8 Saito et al,17 Aldikacti et al,19 and De Pauw et al.21 

The BIC ratio, which expresses the degree of osseointegration, was calculated for 2 of the 10 histologic sections from each implant. The mean BIC values of compression sides of the test and control implants were 57.27% and 55.99%, respectively. These ratios were 62.96% and 64.04% for tension sides of the test and control implants, respectively. These similar BIC ratios of the 2 groups imply that osseointegration would not have been affected by early orthodontic loading, even at forces as high as 500g.

In the present study, the BIC values for tension and compression sides were 62.96% and 57.27%, respectively, for test implants. These values were not significantly different (P > .05). Majzoub et al15 demonstrated after 8 weeks a BIC of 76% on the compression side and 75% on the tension side of implants that had been immediately loaded with 150g of force. Borsos et al25 found higher bone-implant contact (73.1%) in the conventional group than in the immediately loaded group (55.0%). Bone-implant contact of 26% clinically and histologically was classified as successful for immediately loaded implants after 100g force application for 6 months.23 

The percentage of bone density around implants (BV) was assessed from the compression and tension areas of both test and control implants. No significant difference in the percentage of BV was noted between compression and tension sides and between control and test implants. These findings suggest that the early loaded implants maintained rigid osseointegration during orthodontic loading. Saito et al17 reported no statistical difference in BV% between compression and the tension sides and between loaded and unloaded implants. The authors concluded that orthodontic lateral force did not affect osseointegration.17 In the study of Akin-Nergiz et al,14 histologic and morphometric evaluation showed that the density of bone increased with the magnitude of loading.

Bone reacts to a load by adapting its internal and external structure through modeling and remodeling processes. The force applied to the implants activates physiologic bone adaptation and stimulates the remodeling of bone surrounding the implants.7 Histologic analysis of implants is the main method used to elicit details of adaptation, such as qualitative and quantitative bone changes.6 In its histologic analysis, the current study found that the implants had firm contact with the surrounding bone and no intervening connective tissue, especially in the marginal crestal area. This finding supports the findings of many studies.3,7,9,1116,18,19 

Another histologic finding of our study was a more compact bone structure characterized by a slight increase in bone apposition at the marginal crestal areas of the compression sides when compared with the tension sides of control and test implants. This finding supports those of Roberts et al,7 Wehrbein and Diedrich,20 and Majzoub et al.15 However, Wehrbein et al12 reported no bone apposition adjacent to orthodontically loaded implants. They stated that this was due to the fact that the 1 N of force applied was too small to induce marginal osteogenic activity.

Remodeling activity was observed in the present study in the preexisting bone casing of both of the implant groups. These metaplastic changes are a vital mechanism in replacing mature, mechanically loaded, preexisting bone without violating its structural integrity,7,8 and is in accord with the results of previous investigations.12,19 According to these studies, increased remodeling activity was also seen at the loaded test implants when compared with the unloaded control implants.

In histologic sections of both implant groups, it was slightly evident that bone trabeculae were oriented perpendicularly to the compression sides, which apparently corresponded to the lines of stress. This finding supports the findings of Roberts et al.7 

Conclusions

Within the limitations of this study, the following conclusions were drawn: The potential clinical applications of these radiologic and histological results include the possibility of minimizing the healing duration, even for high orthodontic forces, and the possibility of postorthodontic use of these implants as abutments for supporting prosthetic reconstruction.

Abbreviations

     
  • BIC

    bone-implant contact

  •  
  • BV

    bone volume

  •  
  • ISQ

    implant stability quotient

  •  
  • MTX

    microtextured surface

  •  
  • Ni-Ti

    nickel-titanium

References

References
1.
Celenza
F
.
Implants in orthodontics: the impact of new treatment modalities
.
N Y State Dent J
.
2008
;
74
:
52
56
.
2.
Huang
LH
,
Shotwell
JL
,
Wang
HL
.
Dental implants for orthodontic anchorage. Review
.
Am J Orthod Dentofacial Orthop
.
2005
;
127
:
713
722
.
3.
Roberts
WE
,
Marshall
KJ
,
Mozsary
PG
.
Rigid endosseous implant utilized as anchorage to protract molars and close an atrophic extraction site
.
Angle Orthod
.
1990
;
60
:
135
152
.
4.
Odman
J
,
Lekholm
U
,
Jemt
T
,
Thilander
B
.
Osseointegrated implants as orthodontic anchorage in the treatment of partially edentulous adult patients
.
Eur J Orthod
.
1994
;
16
:
187
201
.
5.
Trisi
P
,
Rebaudi
A
.
Progressive bone adaptation of titanium implants during and after orthodontic load in humans
.
Int J Periodontics Restorative Dent
.
2002
;
22
:
31
43
.
6.
Wehrbein
H
,
Merz
BR
,
Hämmerle
CH
,
Lang
NP
.
Bone-to-implant contact of implants in humans subjected to horizontal loading
.
Clin Oral Implants Res
.
1998
;
9
:
348
353
.
7.
Roberts
WE
,
Smith
RK
,
Zilberman
Y
,
Mozsary
PG
,
Smith
RS
.
Osseous adaptation to continuous loading of rigid endosseous implants
.
Am J Orthod
.
1984
;
86
:
95
111
.
8.
Roberts
WE
,
Helm
FR
,
Marshall
KJ
,
Gongloff
RK
.
Rigid endosseous implants for orthodontic and orthopedic anchorage
.
Angle Orthod
.
1989
;
59
:
247
256
.
9.
Turley
PK
,
Kean
C
,
Schur
J
,
et al
.
Orthodontic force application to titanium endosseous implants
.
Angle Orthod
.
1988
;
58
:
151
162
.
10.
Smalley
WM
,
Shapiro
PA
,
Hohl
TH
,
Kokich
VG
,
Branemark
PI
.
Osseointegrated titanium implants for maxillofacial protraction in monkeys
.
Am J Orthod Dentofacial Orthop
.
1988
;
94
:
285
295
.
11.
Linder-Aronson
S
,
Nordenram
A
,
Anneroth
G
.
Titanium implant anchorage in orthodontic treatment: an experimental investigation in monkeys
.
Eur J Orthod
.
1990
;
12
:
414
419
.
12.
Wehrbein
H
,
Glatzmaier
J
,
Yildirim
M
.
Orthodontic anchorage capacity of short titanium screw implants in the maxilla: an experimental study in the dog
.
Clin Oral Implants Res
.
1997
;
8
:
131
141
.
13.
Wehrbein
H
,
Yildirim
M
,
Diedrich
P
.
Osteodynamics around orthodontically loaded short maxillary implants: an experimental pilot study
.
J Orofac Orthop
.
1999
;
60
:
409
415
.
14.
Akin-Nergiz
N
,
Nergiz
I
,
Schulz
A
,
Arpak
N
,
Niedermeier
W
.
Reactions of peri-implant tissues to continuous loading of osseointegrated implants
.
Am J Orthod Dentofacial Orthop
.
1998
;
114
:
292
298
.
15.
Majzoub
Z
,
Finotti
M
,
Miotti
F
,
Giardino
R
,
Aldini
NN
,
Cordioli
G
.
Bone response to orthodontic loading of endosseous implants in the rabbit calvaria: early continuous distalizing forces
.
Eur J Orthod
.
1999
;
21
:
223
230
.
16.
Melsen
B
,
Costa
A
.
Immediate loading of implants used for orthodontic anchorage
.
Clin Orthod Res
.
2000
;
3
:
23
28
.
17.
Saito
S
,
Sugimoto
N
,
Morohashi
T
,
et al
.
Endosseous titanium implants as anchors for mesiodistal tooth movement in the beagle dog
.
Am J Orthod Dentofacial Orthop
.
2000
;
118
:
601
607
.
18.
Melsen
B
,
Lang
NP
.
Biological reactions of alveolar bone to orthodontic loading of oral implants
.
Clin Oral Implants Res
.
2001
;
12
:
144
152
.
19.
Aldikaçti
M
,
Açikgöz
G
,
Türk
T
,
Trisi
P
.
Long-term evaluation of sandblasted and acid-etched implants used as orthodontic anchors in dogs
.
Am J Orthod Dentofacial Orthop
.
2004
;
125
:
139
147
.
20.
Wehrbein
H
,
Diedrich
P
.
Endosseous titanium implants during and after orthodontic load—an experimental study in the dog
.
Clin Oral Implants Res
.
1993
;
4
:
76
82
.
21.
De Pauw
GA
,
Demaut
LR
,
Johansson
CB
,
Martens
G
.
A histomorphometric analysis of heavily loaded and non-loaded implants
.
Int J Oral Maxillofac Implants
.
2002
;
17
:
405
412
.
22.
Higuchi
KW
,
Slack
JM
.
The use of titanium fixtures for intraoral anchorage to facilitate orthodontic tooth movement
.
Int J Oral Maxillofac Implants
.
1991
;
6
:
338
344
.
23.
Borbely
P
,
Dunay
MP
,
Jung
BA
,
Wehrbein
H
,
Wagner
W
,
Kunkel
M
.
Primary loading of palatal implants for orthodontic anchorage: a pilot animal study
.
J Craniomaxillofac Surg
.
2008
;
36
:
21
27
.
24.
Crismani
AG
,
Bernhart
T
,
Schwarz
K
,
Celar
AG
,
Bantleon
H-P
,
Watzek
G
.
Ninety percent success in palatal implants loaded 1 week after placement: a clinical evaluation by resonance frequency analysis
.
Clin Oral Implants Res
.
2006
;
17
:
445
450
.
25.
Borsos
G
,
Rudzki-Janson
I
,
Stockmann
P
,
Schlegel
KA
,
Végh
A
.
Immediate loading of palatal implants in still-growing patients: a prospective, comparative, clinical pilot study
.
J Orofac Orthop
.
2008
;
69
:
297
308
.
26.
Jackson
A
,
Lemke
R
,
Hatch
J
,
Salome
N
,
Gakunga
P
,
Cochran
D
.
A comparison of stability between delayed versus immediately loaded orthodontic palatal implants
.
J Esthet Restor Dent
.
2008
;
20
:
174
185
.
27.
de Cravero Marta
R
,
Carlos
IJ
.
Assessing double acid-etched implants submitted to orthodontic forces and used as prosthetic anchorages in partially edentulous patients
.
Open Dent J
.
2008
;
2
:
30
37
.
28.
Isidor
F
.
Loss of osseointegration caused by occlusal load of oral implants: a clinical and radiographical study in monkeys
.
Clin Oral Implants Res
.
1996
;
7
:
143
152
.