ORIGINAL ARTICLE

Effect of force on alveolar bone surrounding

miniscrew implants: A 3-dimensional
microcomputed tomography study
Christopher C. Massey,a Elias Kontogiorgos,b Reginald Taylor,c Lynne Opperman,d Paul Dechow,d
and Peter H. Buschange
Lubbock and Dallas, Tex

Introduction: The primary aim of this study was to better understand how bone adapts to forces applied to mini-
screw implants. A secondary aim was to determine whether the direction of force applied to miniscrew implants
has an effect on bone surrounding the miniscrew implants. Methods: A randomized split-mouth design, applied
to 6 skeletally mature male foxhound dogs, was used to compare miniscrew implants loaded for 9 weeks with
200 or 600 g to unloaded control miniscrew implants. By using microcomputed tomography, with an isotropic
resolution of 6 mm, bone volume fractions (bone volume/total volume) were calculated for bone around the
entire miniscrew implant surface. Bone volume fractions were calculated for bone 6 to 24, 24 to 42, and 42 to
60 mm from the miniscrew implant surface. For each loaded miniscrew implant, the bone volume fraction was
also calculated for 2 compression and 2 noncompression zones. Results: The 6 to 24-mm layer showed a sig-
nificantly lower (P \0.05) bone volume fraction than did the 24 to 42-mm and the 42 to 60-mm layers, which were
not significantly different. The bone volume fractions of cortical bone surrounding the apical aspects of the un-
loaded miniscrew implants were significantly greater (P \0.05) than the bone volume fractions of cortical bone
surrounding the loaded miniscrew implants. In contrast, the bone volume fractions of noncortical bone surround-
ing loaded miniscrew implants were significantly greater (P \0.05) than the bone volume fractions of bone sur-
rounding the unloaded miniscrew implants. Miniscrew implants loaded with 200 g showed significantly greater
(P \0.05) amounts of noncortical bone volume fractions than did miniscrew implants loaded with 600 g. With
both 200 and 600 g, zones under compression had significantly greater bone volume fractions than did the non-
compression zones. Conclusions: The application of force, the amount of force applied, and the direction of
force all have significant effects on the amounts of bone produced around miniscrew implants. (Am J Orthod
Dentofacial Orthop 2012;142:32-44)

M
iniscrew implants provide skeletal anchorage implants have proven to be versatile in clinical applica-
with minimal need for patient compliance. tions. Despite their many advantages, the survival rates
Their small size makes them easy to place in of miniscrew implants have yet to achieve those of
numerous locations and easy to remove; miniscrew endosseous dental implants.1,2 A recent systematic
review showed that, of 2374 miniscrews (31 different
a
Private practice, Lubbock, Tex. types) placed, 363 failed, resulting in a survival rate of
b
Assistant clinical professor, Restorative Sciences, Baylor College of Dentistry, 84.7%.3 For miniscrew implants to be stable in the
Texas A&M Health Science Center, Dallas. long term, they must be stable immediately after place-
c
Associate professor, Orthodontics, Baylor College of Dentistry, Texas A&M
Health Science Center, Dallas. ment. Movement of miniscrew implants during early
d
Professor, Biomedical Sciences, Baylor College of Dentistry, Texas A&M Health wound healing is considered to be a high risk factor for
Science Center, Dallas.
e
early implant loss.4 Endosseous dental implants have
Professor and director of orthodontic research, Orthodontic Department, Baylor
College of Dentistry, Texas A&M Health Science Center, Dallas. shown that secondary stability—when healing takes
The authors report no commercial, proprietary, or financial interest in the prod- place—is responsible for osseointegration of the
ucts or companies described in this article. implant.5
Reprint requests to: Peter H. Buschang, Orthodontic Department, Baylor College
of Dentistry, Texas A&M Health Science Center, 3302 Gaston Ave, Dallas, TX Our understanding of how bone responds to loading
75246; e-mail, phbuschang@bcd.tamhsc.edu. is based primarily on long bones loaded with heavy,
Submitted, June 2011; revised and accepted, January 2012. intermittent forces. With respect to the dentoalveolar
0889-5406/$36.00
Copyright Ó 2012 by the American Association of Orthodontists. complex, most studies pertain to axial loading of
doi:10.1016/j.ajodo.2012.01.016 endosseous dental implants and show definite effects
32
Massey et al 33

Fig 1. A, Radiographic image showing stent used for miniscrew implant placement; B, radiographic
image confirming intraradicular and interdental placement of miniscrew implants in the posterior man-
dible; C, miniscrew implants placed with immediate loading of 200 g; D, miniscrew implants placed with
immediate loading of 600 g. Note that composite was used to minimize gingival irritation.

of the forces.6-8 However, miniscrew implants place The primary aim of this study was to evaluate with
much lighter, continuous loads on dentoalveolar bone microcomputed tomography the effects of force and
that are transaxial by nature. Because of the force amount on bony adaptations around miniscrew
differences in type, amount, and direction of the load, implants. A secondary aim was to determine whether
research pertaining to dental implants might not apply bone around miniscrew implants subjected to compres-
to miniscrew implants. sive loads adapts differently than does bone around
Studies comparing differences between 2 known unloaded miniscrew implants.
forces have suggested that osseointegration is indepen-
dent of force magnitudes applied to miniscrew
implants.9,10 Studies comparing an applied force with MATERIAL AND METHODS
no force have also shown no significant histologic Six skeletally mature male foxhounds, 1 to 2 years old
differences in bone caused by miniscrew implants.11,12 and weighing between 55 and 65 pounds, were used
Importantly, all of the aforementioned studies for this study. The Institutional Animal Care and Use
evaluated the effects of force on osseointegration with Committee at Baylor College of Dentistry, Dallas, Tex,
histomorphometry, which provides only 2-dimensional approved the care of the animals and the experimental
information for a small portion of the screw.13-15 A protocols. Foxhounds are an established model for
recent study with microcomputed tomography showed investigating peri-implant osseous dynamics; their large
significantly greater bone volume fraction (bone mandibles provide the spaces between miniscrew
volume/total volume) around loaded miniscrew implants necessary for loading.17-20
implants than unloaded miniscrew implants, especially The miniscrew implants (IMTEC, Ardmore, Okla) used
in the noncortical regions.16 These findings suggest were self-drilling, made of titanium alloy, and measured
that microcomputed tomography might be more sensi- 6 mm long and 1.8 mm wide (outer diameter). Each
tive than histomorphometry for evaluating the effects animal had 5 (4 loaded and 1 unloaded) miniscrew
of force on bony adaptations around miniscrew implants. implants placed in the interradicular and interdental

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34 Massey et al

areas of the first and second mandibular molars, with

most having been placed in unattached gingiva. By
using random assignment, the experimental miniscrew
implants on 1 side were loaded with 200 g, and those
on the other side were loaded with 600 g. The unloaded
miniscrew implant was also randomly assigned to 1 side
or the other.
On the day of placement, all animals were sedated
with ketamine (2.2 mg/kg, intramuscularly) and rompin
(0.22 mg/kg, intramuscularly) and given a prophylaxis
with ultrasonic scaling instrumentation. Radiographic
stents were placed, and periapical radiographs were
taken bilaterally to determine miniscrew implant place-
ment locations (Fig 1, A). The radiographic stents were
replaced and used as guides to ensure accuracy of mini-
screw implant placement. All 30 miniscrew implants
were placed in buccal alveolar bone perpendicular to
the cortical plate or parallel to the occlusal plane. The
miniscrew implants were placed in the bifurcations of
the first and second molars. Height and exact anteropos-
terior locations of placement were measured and deter-
mined from periapical radiographs. Unloaded miniscrew
implants were placed approximately 4 mm apical to their
loaded counterparts. Placement sites were marked and
prepared with a 1.5-mm tissue punch, and pilot holes
were drilled by using a 1.1-mm surgical drill under copi-
ous irrigation.
The miniscrew implants were loaded with 200-g Fig 2. A, Original gray-scale 2-dimensional slice with mini-
nickel-titanium coil springs (Dentsply GAC, Bohemia, screw implants in center (white), surrounding bone (gray),
NY) tied through the islets on the heads of the implants and space (black). The volume of interest was defined as
430 pixels in diameter with miniscrew implants in center.
with a 0.010-in stainless steel ligature wire (Fig 1, B).
B, The coronal limit of volume of interest was visually de-
Three 200-g coil springs placed in parallel were used fined as the first slice at which bone was observed com-
to load the miniscrew implants with 600 g (Fig 1, C). pletely surrounding and contacting the miniscrew
The activation forces of the coil springs were measured implants. The apical limit was defined as 10 slices (0.06
with a Correx Gram Force Gauge (Long Island Indicator mm) coronally from the miniscrew implants apex.
Service, Hauppauge, NY). Postoperative peri-implant
sites were irrigated with 0.2% chlorhexidine, and periap- Each bone-implant sample was retrieved with a mod-
ical radiographs were taken bilaterally to ensure proper ified 10-mm diameter trephine bur (ACE Dental Implant
miniscrew implant positioning. Both analgesics (torbu- System, Brockton, Mass) under copious irrigation. The
gesic, 0.2 mg/kg [2 mg/mL with 1 mL per animal]) and samples were sectioned parallel to the long axis of the
antibiotics (penicillin G, 60,000 units/kg) were adminis- implant, ensuring that all 3 layers of the bone (cortical,
tered. Inspection of appliance condition and prophylaxis medullary, and cortical) remained intact and undam-
with a toothbrush and 0.2% chlorhexidine irrigant were aged, and stored in 70% ethanol.
performed weekly. A wet grindstone was used to smooth the outer edges
Nine weeks after miniscrew implant placement, the of the bone-implant specimens to ensure a precise fit
animals were killed with a 2-mL intracardiac injection into the cylindrical (9.8-mm internal diameter) sample
of Beuthanasia-D and perfused with 1 to 2 L of normal holders. A maximum of 3 bone-implant specimens
saline solution, followed by 1 L of 70% ethanol. The were placed in each holder, along with 70% ethanol.
mandibles were resected en bloc and stored in 70% The samples were then radiographically evaluated by us-
ethanol in preparation for the microcomputed tomog- ing microcomputed tomography (35; Scanco Medical,
raphy evaluations. Each hemi-jaw was sectioned to Basserdorf, Switzerland) with an isotropic resolution of
include both the experimental and the unloaded 6 mm. X-ray energy levels were set to 70 kVp, current
miniscrew implants. to 114 mA, and integration time to 800 ms. A 0.5-mm

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Massey et al 35

Fig 3. Three-dimensional reconstructions showing the 3 layers of bone surrounding the miniscrew
implants, including the 6 to 24-mm (white), 24 to 42-mm (purple), and 42 to 60-mm (red) layers. The
0 to 6-mm (black) layer was not evaluated. Cortical and noncortical regions (delimited by green horizon-
tal line) were evaluated separately. Compression and noncompression zones were also evaluated in
the cortical and noncortical regions.

aluminum filter and a high resolution setting of 1000 For each specimen, separate bone volume fractions
projections per 180 were used to ensure the highest were calculated for the cortical and noncortical regions.
quality scans with minimal metal implant artefacts. Bone volume fraction measures the relative amount of
For the 360 analysis of the entire miniscrew implant, bone per unit of volume; for example, a bone volume
a volume of interest for each specimen was defined as fraction ratio of 0.6 indicates 60% bone and 40% space,
430 pixels in diameter with the implant positioned in or nonbone. The analyses pertained to 3 layers of bone,
the center (Fig 2, A). The specific design of the implant 6 to 24, 24 to 42, and 42 to 60 mm from the miniscrew
required the apical limit of the volume of interest to be implant's surface (Fig 4). A previous microcomputed
set to 10 slices (0.06 mm) coronally from the miniscrew tomography study demonstrated the loading effects on
implant's tip (Fig 2, B). The coronal limit of the volume the first 2 layers of bone; the third layer was added in
of interest was visually defined as the slice at which bone our study to more precisely determine the limit of the
was observed to completely surround and contact the loading effects.16 Each layer included 3 voxels (volumet-
miniscrew implant. The average scanning time was 3.2 ric 3-dimensional pixel), each 6 mm thick. The first voxel
hours per specimen. (ie, from 0 to 6 mm from the miniscrew implant) was not
Based on the original gray-scale images, threshold included because it contained most of the metallic hala-
values that produced the best representations of the tion artefacts. For the comparisons of the compression
miniscrew implants, mineralized bone, and background and noncompression zones, the calculated areas of in-
were determined.16 Three-dimensional reconstructions terest included the 6 to 24-mm and the 24 to 42-mm
were generated by using the threshold values. The layers. The 42 to 60-mm layer was not evaluated because
reconstructions of each specimen were divided into preliminary analysis showed no differences between the
a cortical region, which included only cortical bone, outer 2 layers of bone.
and a noncortical region, which included mostly trabec- Four 3-dimensional zones around each miniscrew
ular bone and limited amounts of cortical bone (Fig 3). implant were evaluated to determine whether and how

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36 Massey et al

Fig 4. Original gray-scale 2-dimensional slice showing pie-shaped zones created for evaluating the
effects of compression and noncompression based on the direction of force applied to the miniscrew
implants.

Table I. Linear functions (with scientific notation) describing bone volume fractions* for the 3 layers of cortical and
noncortical bone surrounding unloaded control and loaded (200 g) miniscrew implants
Control 200 g Group difference

Intercept SE Slope SE Intercept SE Slope SE Intercept SE Slope SE

Cortical bone
6-24 mm 5.554e-1 3.928e-2 6.090e-5 8.285e-5 5.952e-1 5.039e-3 1.201e-3 8.704e-5 4.502e-2 4.806e-2 1.063e-3 9.622e-5
24-42 mm 9.893e-1 2.330e-2 1.366e-4 5.689e-5 9.806e-1 3.323e-3 5.582e-4 5.741e-5 4.486e-3 2.849e-2 4.225e-4 6.610e-5
42-60 mm 9.853e-1 2.179e-2 1.560e-4 5.662e-5 9.813e-1 3.189e-3 5.452e-4 5.509e-5 2.566e-4 2.665e-2 3.901e-4 6.575e-5
Noncortical bone
6-24 mm 5.224e-1 3.559e-2 3.202e-3 8.085e-5 4.340e-1 5.819e-3 9.740e-4 1.006e-4 1.040e-1 6.894e-3 2.227e-3 1.017e-4
24-42 mm 9.945e-1 3.521e-2 3.944e-3 9.119e-5 8.875e-1 5.609e-3 1.735e-3 9.696e-5 1.339e-1 7.773e-3 2.208e-3 1.147e-4
42-60 mm 9.937e-1 3.636e-2 4.048e-3 9.841e-5 8.927e-1 5.916e-3 1.967e-3 1.023e-4 1.299e-1 8.388e-3 2.080e-3 1.237e-4

*Intercept (at 0% relative region thickness) 1 (slope $ % relative region thickness).

the direction of applied force influenced the bone. Based separately. Each region included variable numbers of sli-
on the experimental and clinical evidence showing that ces, ranging between 196 and 326 slices for the cortical
miniscrew implants tip with immediate orthodontic region and 292 and 521 slices for the noncortical region.
loading, 2 compression and 2 noncompression zones To make comparisons across the regions, the relative
were digitally created in the same plane of force applica- positions of the slices in each region were standardized
tion.21-24 To create reproducible and standardized zones by dividing each slice number by the total number of
of interest, the cortical and noncortical regions of the slices. This produced the relative position of each slice
volume of interest were digitally divided into 4 equal in each region ranging from 1% to 100%, with 1%
90 pie-shaped zones (Fig 4). Because of the tapered and 100% representing the most coronal and apical
geometry of the miniscrew implants, different vertical slices, respectively.
limits were used to create zones with comparable Multilevel statistical models were used to determine
volumes of bone. the changes between slices in each region, as well as
to evaluate the differences between the unloaded,
200-g, and 600-g groups. The models were developed
Statistical analysis with software (MLwiN; Center for Multilevel Modeling,
The bone surrounding the cortical and noncortical Institute of Education, London, United Kingdom)
regions of the miniscrew implants was evaluated using iterative generalized least squares. The preliminary

July 2012  Vol 142  Issue 1 American Journal of Orthodontics and Dentofacial Orthopedics
Massey et al 37

Table II. Linear functions (with scientific notation) describing bone volume fractions* for the 3 layers of cortical and
noncortical bone surrounding unloaded control and loaded (600 g) miniscrew implants
Control 600 g Group difference

Intercept SE Slope SE Intercept SE Slope SE Intercept SE Slope SE

Cortical bone
6-24 mm 5.554e-1 3.270e-2 6.090e-5 5.887e-5 5.829e-1 2.565e-2 8.880e-4 3.781e-5 2.747e-2 4.003e-2 9.489e-4 6.944e-5
24-42 mm 9.893e-1 1.308e-1 1.366e-4 3.871e-5 9.910e-1 1.051e-2 6.294e-4 2.639e-5 1.635e-3 1.599e-2 4.928e-4 4.566e-5
42-60 mm 9.853e-1 1.156e-2 1.560e-4 3.933e-5 9.907e-1 9.139e-3 5.264e-4 2.661e-5 5.325e-3 1.413e-2 3.704e-4 4.640e-5
Noncortical bone
6-24 mm 5.253e-1 2.197e-2 3.201e-3 6.792e-5 4.015e-1 4.220e-3 1.566e-3 7.295e-5 1.258e-1 7.607e-3 1.635e-3 8.474e-5
24-42 mm 9.376e-1 2.504e-2 3.944e-3 7.820e-5 8.554e-1 4.607e-3 2.079e-3 7.964e-5 6.201e-2 8.756e-3 1.863e-3 9.757e-5
42-60 mm 9.399e-1 2.590e-2 4.048e-3 8.077e-5 8.629e-1 4.822e-3 2.082e-3 8.336e-5 6.501e-2 9.045e-3 1.965e-3 1.008e-4

*Intercept (at 0% relative region thickness) 1 (slope $ % relative region thickness).

Fig 5. Bone volume fraction changes between the most coronal and apical aspects of cortical and
noncortical bones of the control miniscrew implants and the miniscrew implants loaded with 200 g
(based on the equations in Table I). BV/TV, Bone volume fraction.

analysis of the changes of bone volume fractions in both Separate analyses were performed for the cortical and
the cortical and noncortical regions were best described noncortical regions, as well as for the 6 to 24-mm and
by a simple linear regression model. The intercept term 24 to 42-mm layers. Two-level models were used to
described the bone volume fraction at the most coronal partition random variations between specimens and
slice of each region (ie, 0% relative thickness); the slope between zones in each specimen.
described the changes in bone volume fractions for each Multilevel modeling procedures were used because
percent of change of relative slice thickness. For these they make no assumptions as to the equality of the inter-
analyses, 2-level models were used, with random varia- vals used for the independent variable.25 Multilevel pro-
tions partitioned between specimens and between slice cedures made it possible to easily determine the
numbers, within specimens. appropriate curves to use to describe the changes in
Multilevel models were also used to describe and bone volume fractions in a region and simultaneously
compare the compression and noncompression zones. evaluate group differences.25,26

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38 Massey et al

demonstrated significantly (P \0.05) smaller decreases

in bone volume fraction between the coronal and
apical aspects than did the control miniscrew implants.
As a result, there was significantly (P \0.05) less bone
surrounding the apical aspects of the unloaded control
miniscrew implants than the loaded miniscrew
implants (Fig 8).
Only the 6 to 24-mm layer of the cortical region
showed statistically significant differences between
miniscrew implants loaded with 200 and 600 g (Table
III). Although there were no differences at the coronal
aspect, miniscrew implants subjected to 200 g loads
showed significantly (P \0.05) greater decreases in
bone volume fractions between the coronal and apical
aspects. In the noncortical section, miniscrew implants
loaded with 600 g showed significantly (P \0.05)
greater decreases in bone volume fractions than those
Fig 6. Three-dimensional reconstruction of the layers of loaded with 200 g in both the 6 to 24-mm and 24 to
bone: A, 6 to 24 mm and B, 42 to 60 mm from the miniscrew 42-mm layers (Figs 9 and 10).
implant surface (based on the equations in Table II). BV/
There was significantly more bone in the compres-
TV, Bone volume fraction.
sion than in the noncompression zones in both the
cortical and the noncortical regions (Table IV; Fig 11).
RESULTS The differences were highly significant (P \0.001) for
For all miniscrew implants, the cortical regions both the 6 to 24-mm and the 24 to 42-mm layers. In
showed significantly (P \0.05) greater amounts of the cortical region, there was approximately 3% more
bone than did the noncortical regions. All regions bone volume fraction in the compression zone than in
showed significant decreases in bone volume fractions the noncompression zone for both the 6 to 24-mm and
between the most coronal and apical aspects of each the 24 to 42-mm layers of bone. In the noncortical
region, with the exception of the 6 to 24-mm layer in region, there were 7% and 10% greater bone volume
the cortical region of the unloaded miniscrew implants. fractions in the compression zone for the 6 to 24-mm
The decreases were significantly greater in the noncort- and the 24 to 42-mm layers, respectively.
ical regions than in the cortical regions (Tables I and II;
Fig 5).
There were no significant (P \0.05) differences in DISCUSSION
bone volume fractions between the 24 to 42-mm and There was less noncortical than cortical bone sur-
the 42 to 60-mm layers of bone. By contrast, the 6 to rounding the control miniscrew implants; the noncorti-
24-mm layer showed significantly (P \0.05) less bone cal regions also showed greater decreases in bone
than did the 24 to 42-mm and the 42 to 60-mm layers between the coronal and apical aspects of the miniscrew
(Fig 6). implants than did the cortical bone. The cortical and
In the coronal aspect of the cortical region, there was noncortical regions of the loaded and unloaded screws
no statistically significant (P \0.05) difference in bone showed 1%, and 32% to 40% decreases in bone volume
volume fractions between the unloaded control and fractions, respectively, between their most coronal and
loaded miniscrew implants (Tables I and II). The loaded apical slices. Ikeda et al16 also showed a decreasing
miniscrew implants showed significantly (P \0.05) pattern of bone volume fraction in both the cortical
greater decreases in bone volume fractions between and the noncortical regions, with the noncortical region
the coronal and apical aspects. As a result, the loaded having greater decreases. Ohmae et al11 also reported
miniscrew implants had significantly less bone apically smaller decreases in the amount of bone between the
than did the the unloaded control miniscrew implants coronal and middle thirds than between the middle
(Figs 5 and 7). and apical thirds. The inherent differences in macro-
There was significantly more control bone surround- architecture between cortical and trabecular bone are
ing the coronal aspects of miniscrew implants in the well established; cortical bone is a much denser, compact
noncortical regions (Tables I and II). In contrast to bone, whereas trabecular bone is less dense, spongy,
the cortical regions, the loaded miniscrew implants or cancellous. Cancellous bone is, by definition,

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Massey et al 39

Fig 7. Bone volume fraction changes between the most coronal and apical aspects of cortical and
noncortical bones of control miniscrew implants and miniscrew implants loaded with 600 g. BV/TV,
Bone volume fraction.

Table III. Linear functions (with scientific notation) describing bone volume fractions* for the layers of cortical and
noncortical bone surrounding miniscrew implants loaded with 200 and 600 g
200 g 600 g Group difference

Intercept SE Slope SE Intercept SE Slope SE Intercept SE Slope SE

Cortical bone
6-24 mm 5.952e-1 5.039e-3 1.201e-3 8.704e-5 5.829e-1 2.565e-2 8.880e-4 3.781e-5 1.757e-2 4.083e-2 3.142e-4 6.700e-5
24-42 mm 9.806e-1 3.323e-3 5.582e-4 5.741e-5 9.910e-1 1.051e-2 6.294e-4 2.639e-5 6.138e-3 2.230e-2 7.029e-5 4.713e-5
42-60 mm 9.813e-1 3.189e-3 5.452e-4 5.509e-5 9.907e-1 9.139e-3 5.264e-4 2.661e-5 5.078e-3 2.051e-2 1.971e-5 4.693e-5
Noncortical bone
6-24 mm 4.340e-1 5.819e-3 9.740e-4 1.006e-4 4.015e-1 4.220e-3 1.566e-3 7.295e-5 2.870e-2 5.160e-2 5.922e-4 8.216e-5
24-42 mm 8.875e-1 5.609e-3 1.735e-3 9.696e-5 8.554e-1 4.607e-3 2.079e-3 7.964e-5 2.875e-2 4.934e-2 3.453e-4 8.791e-5
42-60 mm 8.927e-1 5.916e-3 1.967e-3 1.023e-4 8.629e-1 4.822e-3 2.082e-3 8.336e-5 2.900e-2 5.085e-2 1.157e-4 9.458e-5

*Intercept (at 0% relative region thickness) 1 (slope $ % relative region thickness).

discontinuous. The decreases observed in the noncorti- of miniscrew implant placement into highly dense, com-
cal regions indicate that cancellous bone becomes pro- pact bone. It has been suggested that strains above
gressively more porous away from the endosteal surface. 25,000 microstrain exceed the ultimate fracture strength
In the cortical region, loaded miniscrew implants had of bone, leading to microfractures.28 Recent finite
approximately 3% less bone than the unloaded mini- element analyses indicate that strains produced during
screw implants. Luzi et al27 also reported significantly miniscrew implant placement are substantially greater
greater bone volume fractions (6%) for unloaded mini- than 25,000 microstrain.29 Such strain levels might be
screw implants than for those loaded with 50 cN after expected to produce microdamage well beyond the
8 weeks of healing, but their data included both cortical bone-miniscrew implant interface. Microdamage has
and noncortical bone. These results suggest that there been demonstrated as far as 200 mm from the miniscrew
might be an interaction between the forces applied to implant, suggesting severe destruction associated with
the miniscrew implants after insertion and the effects the placement of miniscrew implants, even when pilot

American Journal of Orthodontics and Dentofacial Orthopedics July 2012  Vol 142  Issue 1
40 Massey et al

more rapid healing and remodeling.34 Without extensive

compression resulting from miniscrew implant insertion,
loading can increase bone apposition in the noncortical
area because of its ability to limit micromotion, which
has been shown to contribute to fibrous repair of bone
around miniscrew implants.4 Using a novel in-vivo
model, Willie et al35 recently demonstrated enhanced
cancellous bone osseointegration by limiting micromo-
tion during mechanical loading.
The larger 600-g load produced significantly less
bone in the noncortical region than did the 200-g
load. This difference suggests that the heavier loads
may be approaching Frost’s proposed microdamage
threshold.28 If the physiologic limit of damage had
been reached by introducing more strain through con-
tinuous loading, even less bone gain would be expected
with increasingly larger loads. Also, it has been shown
that the extent of miniscrew implant tipping is directly
related to the amount of force applied, with more force
resulting in more tipping, and it is reasonable to assume
Fig 8. Three-dimensional reconstruction of the layer of
bone 6 to 24 mm from the miniscrew implants surfaces greater compression with greater tipping.24 Another
of A, unloaded controls and B, miniscrew implants loaded possible explanation is that the damage caused by mini-
with 200 g. BV/TV, Bone volume fraction. screw implant insertion has weakened the noncortical
bone to such an extent that the larger load produces
holes were drilled.30 Chen et al31 showed that heavily less bone gain. These slight but significant differences
fractured cortical bone is produced after punching holes between force loads might differ, depending on factors
with mini-microfracture awls. They noted that microfrac- such as implant geometry or surface characteristics
tures indicated extreme compression caused by that were not compared in our study.
mechanical shearing and crushing of bone; the compres- There was significantly less bone in the 6 to 24-mm
sion induced substantial osteocyte necrosis and sealed layer compared with the 24 to 42-mm and the 42 to
off the marrow blood supply. It has been well docu- 60-mm layers, which showed no differences. This
mented that the mircocracks seen in cortical bone after suggests that bone remodeling begins at a distance
the insertion of miniscrew implants are a result of severe from the miniscrew implants. Morinaga et al,36 using
compression of the highly dense compact bone; this leads similar microcomputed tomography settings (7-mm
to local ischemia and bone necrosis.32,33 When extensive resolution) to evaluate bone volume fractions around
damage of bone occurs during miniscrew implants miniscrew implants, showed that bone formation started
insertion, a subsequent orthodontic load could 30 to 50 mm from the bone-implant interface after
exacerbate the damage, thereby limiting bone formation. approximately 5 days and progressed toward the implant
In contrast to the cortical sections, the loaded mini- over the subsequent 23 days. If bone formation starts
screw implants showed significantly more bone than around 30 to 50 mm from the miniscrew implant surface,
the unloaded miniscrews in the noncortical regions. the bone volume fraction between the 24 to 42-mm and
Although microdamage associated with implant inser- the 42 to 60-mm layers might be expected to be similar
tion has not been evaluated in trabecular bone, it is after 9 weeks of healing. These layers might also be
reasonable to assume that there is far less compression expected to be more ossified than the 6 to 24-mm layer.
during insertion in trabecular than in cortical bone. These findings also support the theoretical model pro-
Our results suggest that the strains produced were below posed for endosseous implants, which attributes most
the “fatigue damage strain ranges” of Frost,28 allowing of the healing to distance osteogenesis as opposed to
for functional bone apposition. Not only might com- contact osteogenesis.37,38
pression in the noncortical region be expected to be The differences in bone volume fraction seen in the
much lower, but subsequent healing might also be 6 to 24-mm layer are actual differences that are probably
expected to be much faster than in cortical bone. Can- not related to scatter or metallic halation artefacts. This
cellous bone has a high surface area for osteogenic cell contention is based on 4 lines of reasoning. First, previ-
attachment and a rich vasculature, both of which ensure ous studies that restricted their regions of interest to

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Massey et al 41

Fig 9. Bone volume fraction changes between the most coronal and apical aspects of cortical and
noncortical bones for miniscrew implants loaded with 200 and 600 g. BV/TV, Bone volume fraction.

Table IV. Comparisons of bone volume fractions of

the compression and noncompression zones in the
cortical and noncortical regions of loaded miniscrew
implants, with separate estimates for the 6 to 24-mm
and the 24 to 42-mm layers
Compression Noncompression Difference

Estimate SE Estimate SE Estimate SE

Cortical bone
6-24 mm 0.569 0.019 0.540 0.022 0.029 0.008
24-42 mm 0.973 0.007 0.945 0.014 0.027 0.006
Noncortical bone
6-24 mm 0.385 0.045 0.321 0.044 0.065 0.006
24-42 mm 0.787 0.051 0.687 0.063 0.101 0.007

bone beyond some set distance from the implant did so

based on findings of greater amounts of bone closest to
the implant.15,16,39 The exclusion was necessary due to
the halation artefact that overestimated the amount of
bone closest to the implant. In contrast, in this study, Fig 10. Three-dimensional reconstruction of the layer of
we showed less bone in the layer closest to the bone 6 to 24 mm from the screws’ surface for miniscrew
miniscrew implants. Second, the 6 to 24-mm layer implants loaded with A, 200 g and B, 600 g. BV/TV,
showed bone changes similar to those observed in the Bone volume fraction.
layers farther from the miniscrew implants. Third,
previous studies had poorer resolutions (24-30 mm) an isotropic resolution of 6 mm and a 6-mm long tapered
and used much larger cylindrical implants (length, miniscrew implant with a maximum diameter of
10-13 mm; diameter, 3.5-4.2 mm) than we did, with 1.8 mm.16,39 Finally, the miniscrew implants used in

American Journal of Orthodontics and Dentofacial Orthopedics July 2012  Vol 142  Issue 1
42 Massey et al

Fig 11. A, Bone volume fraction (mean 6 1 SD) of cortical bone in the compression and noncompres-
sion zones; B, bone volume fraction (mean 6 1 SD) of noncortical bone in the compression and
noncompression zones. BV/TV, Bone volume fraction.

our study produced a minor halation effect within the implants have shown no differences.10,11,13,40
first 6 mm from the miniscrew implant's surface; this However, these studies performed histologic
was not included in the analyses. evaluations, which, as initially indicated, are limited in
There is both experimental and clinical evidence that their ability to identify differences. Our findings are
miniscrew implants tip with immediate orthodontic consistent with orthopedic literature showing bone
loading, with a center of rotation probably located in “compaction” in response to compression, with
the more dense cortical region.21-24 The zones under resultant increases in bone volume.31
compression showed 3% to 10% more bone than The clinical applicability of these results is directly
did the noncompression zones, especially in the related to the similarity of canine and human bones. It
noncortical sections. Greater bone in the noncortical has been shown that the composition (ash weight,
sections might be due to greater amounts of miniscrew hydroxyproline, extractable proteins, IGF01) and the
implant displacement, producing greater compression density of human bones are more closely approximated
than in the cortical sections. Greater miniscrew implant by canine bones than by sheep, pig, cow, and chicken
displacement and greater bony compression might be bones.41,42 Bone formation in dogs has been estimated
expected to occur at sites farther from the center of to be approximately twice that of humans,43 and remod-
rotation. With the exception of 1 study,13 all previous eling is approximately 42% faster than in humans.44
studies evaluating the effects of compression vs Canine bone is also denser than human bone.45 Never-
noncompression on bone volume around miniscrew theless, the similarities between canine and human

July 2012  Vol 142  Issue 1 American Journal of Orthodontics and Dentofacial Orthopedics
Massey et al 43

bones have led authors to conclude that, with the excep- anchors for orthodontic intrusion in the beagle dog. Am J Orthod
tion of other primates, the bones of dogs have the most Dentofacial Orthop 2001;119:489-97.
12. Freire JN, Silva NR, Gil JN, Magini RS, Coelho PG. Histomorpho-
similar structure to that of humans.41,46
logic and histomophometric evaluation of immediately and early
loaded mini-implants for orthodontic anchorage. Am J Orthod
CONCLUSIONS Dentofac Orthop 2007;131:704.e1-9.
13. Vande Vannet B, Sabzevar MM, Wehrbein H, Asscherickx K.
1. Loaded miniscrew implants displayed less bone than Osseointegration of miniscrews: a histomorphometric evaluation.
unloaded miniscrew implants in the cortical regions, Eur J Orthod 2007;29:437-42.
14. Butz F, Ogawa T, Chang TL, Nishimura I. Three-dimensional bone-
but more bone than unloaded miniscrew implants in
implant integration profiling using micro-computed tomography.
the noncortical regions. Int J Oral Maxillofac Implants 2006;21:687-95.
2. Larger loads (600 g) produced less bone in the 15. Stoppie N, van der Waerden JP, Jansen JA, Duyck J, Wevers M,
noncortical regions than smaller loads (200 g). Naert IE. Validation of microfocus computed tomography in the
3. The layer of bone closest to the miniscrew implants evaluation of bone implant specimens. Clin Implant Dent Relat
Res 2005;7:87-94.
(6-24 mm) showed less bone than the layers farther
16. Ikeda H, Rossouw PE, Campbell PM, Kontogirogos E,
away (24-42 and 42-60 mm). Buschang PH. Three-dimensional analyses of peri-bone-implant
4. There were no differences in the amounts of bone contact of rough-surface mini-screw implants. Am J Orthod
between the 24 to 42-mm and the 42 to 60-mm Dentofacial Orthop 2011;139:e153-63.
layers. 17. Cochran DL, Schenk RK, Lussi A, Higginbottom FL, Buser D. Bone
response to unloaded and loaded titanium implants with a sand-
5. Cortical and noncortical zones under compression
blasted and acid-etched surface: a histometric study in the canine
exhibit greater amounts of bone than do zones mandible. J Biomed Mater Res 1998;40:1-11.
not under compression. 18. Bakaeen L, Quinlan P, Schoolfield J, Lang NP, Cochran DL. The
biologic width around titanium implants: histometric analysis of
the implantogingival junction around immediately and early loaded
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