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European Journal of Orthodontics 35 (2013) 583589 The Author 2012.

or 2012. Published by Oxford University Press on behalf of the European Orthodontic Society.
doi:10.1093/ejo/cjs066 All rights reserved. For permissions, please email: journals.permissions@oup.com
Advance Access publication 4 October 2012

Effect of the quantity and quality of cortical bone on the failure


force of a miniscrew implant
MasahiroIijima*, MasamitsuTakano**, YoshitakaYasuda***, TakeshiMuguruma*,
SusumuNakagaki*, YasunoriSakakura****, MorioOchi** and ItaruMizoguchi*
*Division of Orthodontics and Dentofacial Orthopedics, Department of Oral Growth and Development, School of
Dentistry, **Division of Fixed Prosthodontics and Oral Implantology, Department of Oral Rehabilitation, Health
Sciences University of Hokkaido, Ishikari-Tobetsu, Hokkaido, ***Yasuda Orthodontic Office, Nishinomiya, Hyogo,
and ****Division of Anatomy, Department of Oral Growth and Development, School of Dentistry, Health Sciences
University of Hokkaido, Ishikari-Tobetsu, Hokkaido, Japan

Correspondence to: Masahiro Iijima, Division of Orthodontics and Dentofacial Orthopedics, Department of Oral
Growth and Development, School of Dentistry, Health Sciences University of Hokkaido, Kanazawa 1757, Hokkaido
061-0293, Japan. E-mail: iijima@hoku-iryo-u.ac.jp

summary This study examined the influence of the quantity and quality of cortical bone on the failure
force of miniscrew implants. Twenty-six titanium alloy miniscrew implants (AbsoAnchor) 1.4mm in diam-
eter and 5 or 7mm long were placed in cross-sectioned maxillae (n=6) and mandibles (n=20) of human
cadavers. Computed tomography imaging was used to estimate the cortical bone thickness and bone
mineral density [total bone mineral density (TBMD, values obtained from cortical bone plus trabecular
bone); cortical bone mineral density (CBMD, values obtained from only cortical bone)]. Maximum force
at failure was measured in a shear test. Nanoindentation tests were performed to measure the hardness
and elastic modulus of cortical bone around the miniscrew implants. The mean failure force of miniscrew
implants placed in mandibles was significantly greater than that for implants in maxillae, and the bone
hardness of mandibles was significantly greater than that of maxillae. The length of miniscrew implants
did not influence the mean failure force in monocortical placement in the mandible. Cortical bone thick-
ness, TBMD, CBMD, and bone hardness were significantly related to the mean failure force. CBMD was
related to the mechanical properties of cortical bone. In conclusion, the quantity and quality of cortical
bone greatly influenced the failure force of miniscrew implants.

Introduction
loading may improve the success rate of miniscrew implants
Miniscrew implants have been gaining popularity because because cyclic mechanical forces have been shown to
their small size allows for more placement sites in the modulate the development and regeneration of bone (Turner
oral cavity, less discomfort for patients, an easy surgical etal., 1994; Robling etal., 2001).
procedure, and low cost (Miyawaki etal., 2003; Park etal., The primary stability of miniscrew implants has been
2006; Kuroda etal., 2007). For the proper application of attributed to mechanical factors (mechanical locking) in
miniscrew implants, clinicians expect reliable anchorage the initial stage. To investigate the mechanical locking of
without the need for patient compliance. However, one of miniscrew implants and bone, mechanical tests such as a
the major concerns regarding miniscrew implants is their tension test (pull-out test; Pickard etal., 2010) and shear
relatively high failure rate. Arecent systematic review article test (tangential loading test; Morarend etal., 2009; Lemieux
showed that the failure rate of miniscrew implants ranged etal., 2011) have been previously used; some studies have
from 13.4 to 20.1 per cent (Schtzle etal., 2009). Many used human cadavers (Morarend etal., 2009; Pickard etal.,
factors, including implant dimension (Miyawaki etal., 2003; 2010; Lemieux etal., 2011), since the absolute values of
Morarend etal., 2009), implant length (Lemieux etal., 2011), the properties of the bone material of mammals differ con-
insertion orientation (Pickard etal., 2010), insertion torque siderably (Zioupos etal., 1999). The mechanical locking of
(Motoyoshi etal., 2010), cortical bone thickness (Huja etal., miniscrew implants may be influenced by bone quantity and
2005; Motoyoshi etal., 2009), and bone mineral density bone quality, which have been evaluated using the cortical
(BMD; Santiago etal., 2009; Cha etal., 2010), have been bone thickness (Huja etal., 2005; Baumgaertel etal., 2009;
reported to influence the stability of miniscrew implants. Motoyoshi etal., 2009) or BMD (Santiago etal., 2009; Cha
On the other hand, a recent study showed that cortical bone etal., 2010). Seong etal. (2009) reported that, in human
thickness decreases during the healing period because of cadavers, the mechanical properties (hardness and elastic
bone resorption around the miniscrew implant (Salmria modulus) of the maxilla and mandible were different. The
etal., 2008). The immediate application of orthodontic bone hardness and elastic modulus are influenced by the
584 M. IIJIMA ET AL.

mineral content and crystal structure, and these may be Table1 List of human cadavers used in this study.
associated with the clinical primary stability of a miniscrew
implant. However, little is known about the relationship Cadavers Mandible Mandible Maxillae Age
between the primary stability of miniscrew implants and the (5mm) (7mm)
hardness and elastic modulus of corticalbone.
The purpose of this study was to investigate the influ- 1 76
2 67
ence of the quantity and quality of cortical bone, such as 3 82
the thickness, BMD, hardness, and elastic modulus, on the 4 74
force required for failure of miniscrew implants placed in 5 74
6 58
human cadavers. We hypothesized that the hardness and 7 85
elastic modulus of cortical bone do not affect the failure 8 58
force of miniscrew implants and that BMD is related to the 9 85
10 77
mechanical properties of bone. 11 53

12 78
13 51
Materials and methods 14 67
15 85
Under the permission of domestic law, the human cadav- 16 56
ers have been donated to the Health Sciences University of
Hokkaido for dental education and research. Fourteen man- , male; , female.
dibles and four maxillae from 16 cadavers were obtained
for the present study after the cadavers had been used for
anatomical dissection by dental students. Fully dentate and rotation, and a slice thickness of 1.0mm with a high-
partially dentate specimens were considered to be accept- resolution mode before and after the miniscrew implants
able. The average age of the cadavers was 70.4years (51 were placed (Prospeed FII, GE). The CT data were saved
85years); 72.9years (5885years) for male and 68.3years as Digital Imaging and Communication in Medicine files,
(5185years) for females. After the mandibles and maxillae and 3D reconstructed images of the specimens were made
were sectioned, soft tissue was carefully removed. using SimPlant Pro 12.03 (Materialise, Leuven, Belgium).
The region between the second premolar and first molar The cortical bone thickness was measured by using images
was sectioned with a water-cooled diamond-saw (MG4000, after implantation of the miniscrew implant (Figure1a). The
Exakt, Nordsteds, Germany). The samples with missing BMD values per area [total bone mineral density (TBMD,
teeth (both second premolar and first molar) were excluded values obtained from cortical bone plus trabecular bone:
in the present study. For mechanical testing, all samples areas of 1.5 5mm or 1.5 7mm); Cortical bone mineral
were ground with 600 grit sandpaper to a thickness of density (CBMD, values obtained from only cortical bone)]
approximately 10mm. One or two cross-sectioned speci- in Hounsfield units were also determined from images
mens of mandible and maxillae were obtained from each before the placement of miniscrew implants using the
human cadaver. The list of human cadavers used in this software (Figure1b).
study is shown in Table1. The maximum force at failure in the shear test (failure
Twenty-six as-received titanium alloy miniscrew force) for each miniscrew implant was measured with a uni-
implants (AbsoAnchor, Dentos, Daegu, Korea) 1.4mm in versal testing machine (EZtest, Shimadzu, Kyoto, Japan).
diameter and 5 or 7mm long were used. The miniscrew Agrip was used to hold the specimens and the position of
implants 5mm long were used for both mandibular (n=11) the specimen was adjusted so that a knife-edged shearing
and maxillary specimens (n=6). To compare miniscrew blade was secured to the crosshead with the direction of
implants with different lengths, nine miniscrew implants force parallel to the bone surface (Figure1c). The shear test
7mm long were used for mandibular specimens with com- was carried out at a crosshead speed of 1mm per minute.
paratively thick bucco-lingual diameters to avoid bicortical Nanoindentation tests were carried out to measure the
support. All miniscrew implants were placed in the buccal mechanical properties of cortical bone around the minis-
alveolar bone by the same operator (Y.Y.) after an approxi- crew implants after shear testing (ENT-1100a, Elionix,
mately 2mm deep pilot hole was made with a slow-speed Tokyo, Japan). All of the specimens were ground to be
handpiece and a pilot drill 1.1mm in diameter according to approximately 5mm thick, using 600 grit sandpaper. All
the manufactures recommendation. All miniscrew implants nanoindentation testing was carried out at 28C with a peak
were placed perpendicular to the buccal bone surface. load of 100 mN using a Berkovich indenter. For each speci-
To measure the buccal cortical bone thickness and BMD men, five indentations were placed on the cortical bone
of the area that contained miniscrew implants, computed without damage by implant failure and the mean hardness
tomography (CT) images were taken under a 200mm field and elastic modulus were calculated by software provided
of view, 120kV, 130 mA, scanning time of 1.0 seconds/ with the nanoindentation apparatus (Figure1d).
PRIMARY STABILITY OF AMINISCREW IMPLANT 585

Figure1 The series of experiments in the present study. (a and b) Estimation of buccal cortical bone thickness and bone mineral den-
sity using the computed tomography and SimPlant Pro; (c) shear testing of a placed miniscrew implant; and (d) nanoindentation test for
a polished specimen to estimate the bone hardness and elastic modulus.

Statistical analysis
The experimental results were analyzed using IBM SPSS
Statistics software (version 19.0J for Windows, IBM,
Armonk, New York, USA). The data of mean failure force,
buccal bone thickness, TBMD, CBMD, hardness, and
elastic modulus, along with the standard deviation, for
each group was normally distributed (ShapiroWilk test).
However, the values were compared using the Kruskal
Wallis test and the MannWhitney U-test since the number
of samples was different among groups. Significances
were predetermined at P<0.0167 for comparison of the
failure force, buccal bone thickness, TBMD, and CBMD,
and P<0.05 for comparison of the hardness and elastic
modulus. The relationships among the above factors were
investigated with the Pearson correlation coefficient test. Figure2 Failure force in the shear test in the three specimen groups.
Horizontal bars in boxes are medians; 50% of all values are within boxes.
Bottom and top of each box indicate lower and upper quartiles, respec-
Results tively. Vertical lines represent complete range of values.
The results regarding mean failure force, cortical bone
thickness, TBMD, and CBMD are shown in Figures 24; did not find significant differences in cortical bone thick-
the detailed values are summarized in Table2. The Kruskal ness (P=0.181) or TBMD (P=0.149) among the three
Wallis test showed a significant difference in failure force specimen groups. The mean failure forces of both 5 and
(P=0.001) and CBMD (P=0.004) among the three speci- 7mm miniscrew implants in the mandible were signifi-
men groups. On the other hand, the three specimen groups cantly greater than that of 5mm implants in the maxillae,
586 M. IIJIMA ET AL.

hardness, and bone elastic modulus in the three specimen


groups. The mean cortical bone thickness (r=0.529),
TBMD (r=0.555), CBMD (r=0.490), and bone hardness
(r=0.400) were significantly related to the failure force in
the shear test. The mean CBMD was significantly related
to the hardness (r=0.446) and elastic modulus (r=0.445).

Discussion
The absolute values of the properties of bone material
in mammals differ considerably (Zioupos etal., 1999).
Therefore, this study used human cadavers to investigate
the failure force of miniscrew implants, which is believed
to be strongly influenced by bone quantity and bone quality.
Age affects the properties of bone in animals and humans
Figure3Cortical bone thickness in the three specimen groups. (Zioupos etal., 1999). In general, with age there is an
Horizontal bars in boxes are medians; 50% of all values are within boxes. increase in the mineral content of the bone tissue, which
Bottom and top of each box indicate lower and upper quartiles, respec-
tively. Vertical lines represent complete range of values.
achieves its best strength and stiffness at maturity (Zioupos
etal., 1999). However, Burstein etal. (1976) measured the
mechanical properties of cortical bone specimens from
although there was no significant difference between speci- human femora and tibiae for a population ranging in age
mens with different lengths (5 and 7mm) in the mandible. from 21 to 86years; reported that no significant differences
The mean CBMD of 7mm miniscrew implants in the man- were found between the mechanical properties of male and
dible was significantly greater than that of 5mm implants in female specimens. Therefore, the results obtained in the
the maxillae, although there was no significant difference present study are worthwhile, although the age of cadavers
between 5mm implants in the mandible and maxillae. were extremely different from general orthodontic patients.
The results regarding mean cortical bone hardness and Lemieux etal. (2011) compared the tensile strength of
elastic modulus are shown in Table3. The mean bone hard- miniscrew implants of different lengths (6, 8, and 10mm)
ness for mandibular specimens was significantly greater and found that longer miniscrew implants provide greater
than that for maxillary specimens (P=0.001). Similarly, anchorage; however, longer miniscrew implants (8 and
the mean bone elastic modulus for mandibular specimens 10mm) were associated with a greater incidence of sinus
was significantly greater than that for maxillary specimens and bicortical perforations (Lemieux etal., 2011). Although
(P=0.003). the primary stability of miniscrew implants can be improved
Table4 shows the correlations among the mean fail- by bicortical placement using longer implants, evaluation
ure force, cortical bone thickness, TBMD, CBMD, bone by CT imaging is required to avoid risks such as touching

Figure4 Bone mineral density in Hounsfield units in the three specimen groups. (a) TBMD and (b) CBMD. Horizontal bars in boxes are medians; 50%
of all values are within boxes. Bottom and top of each box indicate lower and upper quartiles, respectively. Vertical lines represent complete range of values.
PRIMARY STABILITY OF AMINISCREW IMPLANT 587

Table2 Mean failure force, cortical bone thickness, total bone mineral density (TBMD), and cortical bone mineral density (CBMD)
obtained in maxillary and mandibular specimens.

Mandible (5mm) Mandible (7mm) Maxillae P value

Mean Standard Mean Standard Mean Standard


deviation deviation deviation

Failure force (N) 182.47a 51.44 143.95a 30.72 70.30b 26.42 0.001
Cortical bone thickness (mm) 1.90 0.96 2.31 0.78 1.40 0.31 0.181
TBMD (HU; cortical bone plus 1124.47 303.6 1134.63 290.25 831.89 296.89 0.149
trabecular bone)
CBMD (HU; cortical bone) 1541.44a,b 244.07 1771.25a 202.9 1199.39b 375.66 0.004

The values were compared using the KruskalWallis test and the MannWhitney U-test (P<0.0167). Identical letters indicate that mean values were not
significantly different.

Table3 Mean hardness and elastic modulus obtained in


maxillary and mandibular specimens. (2010) reported that the CBMD significantly influenced the
primary stability of miniscrew implants. In the present study,
although there was no significant difference in the buccal
Mandible Maxillae P value
bone thickness or TBMD among the three specimen groups
Mean Standard Mean Standard due to individual variation, the mean buccal bone thickness
deviation deviation (r=0.529), TBMD (r=0.555), and CBMD (r=0.490) in
Pearson correlation coefficient test (two mandibular groups
Hardness (GPa) 0.64 0.11 0.42 0.10 0.001
Elastic modulus 24.41 5.00 18.14 2.94 0.003 were combined into one group) were significantly related
(GPa) to the mean failure force, which corresponds to the primary
stability of miniscrew implants. The primary stability of
MannWhitney U-test (P<0.05). miniscrew implants may also be influenced by the mechani-
cal properties of bone, such as its hardness and elastic mod-
ulus. Therefore, the present study used the nanoindentation
the root and sinus and bicortical perforation of lingual bone test to characterize the mechanical properties of bone. With
(Morarend etal., 2009). On the other hand, in the present the nanoindentation technique, it is possible to determine
study, miniscrew implants of two different lengths (5 and the hardness and elastic modulus simultaneously (Pharr and
7mm) were compared with regard to the failure force in the Oliver, 1989; Oliver and Oharr, 1992; Iijima etal., 2011).
shear test, and there was no significant difference in fail- The nanoindentation tests have allowed the measurement
ure force between the two lengths of miniscrew implants of mechanical properties for extremely small volumes of
when placed in mandibular bone. In addition, CT images materials where the contact radius is less than 100nm and
confirmed that none of the specimens showed bicortical the indentation in the present study were placed carefully
placement. These results may suggest that unless bicortical on the cortical bone without cracking to avoid the effects of
placement is used, a long miniscrew implant is unnecessary. bone damage by implant failure.
The orientation of a miniscrew implant also influences The results of the nanoindentation test showed that there
its primary stability. Pickard etal. (2010) reported that was a significant correlation between the mean failure force
the highest concentration of stress could be expected at in the shear test and bone hardness. However, the elastic
an angle of 45 degrees near the cortical surface of bone modulus of bone was not significantly correlated with
in shear tests of miniscrew implants angled at 45 degrees the failure force. In addition, the mean bone hardness of
away (tent-pegged) from the line of force, and this stress mandibular specimens was significantly greater than that of
concentration resulted in a reduction in miniscrew implant maxillary specimens, which agrees with a previous finding
stability and resistance to failure. In addition, another (Zioupos etal., 1999); and thus mandibular bone is more
previous study by Morarend etal. (2009) reported that resistant to deformation and can bear more load under
larger-diameter miniscrew implants provided increased clinical conditions. In the present study, the failure force in
anchorage force resistance compared with smaller-diameter shear testing determined for the mandible was significantly
monocortical miniscrew implants, although larger diameter greater than that for maxillae. However, previous studies
of the miniscrew implants have a higher risk of touching the have reported a lower clinical success rate with miniscrew
root (Kuroda etal., 2007). implants in the mandible (Park etal., 2006; Wu etal.,
The quantity and quality of a cortical bone may influence 2009). The reasons for the lower clinical success rate in
the long-term stability of a miniscrew implant. Cha etal. the mandible may be that the inflammation of peri-implant
588 M. IIJIMA ET AL.

Table4 Pearsons correlation coefficient (r) among failure force, cortical bone thickness, bone mineral density (BMD), hardness, and
elastic modulus.

Failure force Cortical bone TBMD (cortical bone CBMD (cortical Hardness Elastic modulus
thickness plus trabecular bone) bone)

Failure force 1
Cortical bone 0.529** 1
thickness
TBMD (cortical bone 0.555** 0.769*** 1
plus trabecular bone)
CBMD (cortical bone) 0.490 *
0.664 ***
0.672*** 1
Hardness 0.400* 0.426* 0.326 0.446* 1
Elastic modulus 0.311 0.246 0.126 0.445* 0.430* 1

CBMD, cortical bone mineral density; TBMD, total bone mineral density.
*
P<0.05, **P<0.01, ***P<0.001.

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