Journal of Biomechanics 47 (2014) 3–13

Contents lists available at ScienceDirect

Journal of Biomechanics
journal homepage: www.elsevier.com/locate/jbiomech
www.JBiomech.com

Review

Biomechanical determinants of the stability of dental implants:

Influence of the bone–implant interface properties
Vincent Mathieu a, Romain Vayron a, Gilles Richard b, Grégory Lambert b, Salah Naili a,
Jean-Paul Meningaud c, Guillaume Haiat d,n
a
Université Paris-Est, Laboratoire Modélisation et Simulation Multi Echelle, UMR CNRS 8208, 61 avenue du Général de Gaulle, 94010 Créteil cedex, France
b
Septodont, 58 Rue Pont de Créteil, 94100 Saint-Maur-des-Fossés, France
c
Service de Chirurgie Plastique, Reconstructrice et Esthétique, CHU H. Mondor, 94017 Créteil cedex, France
d
CNRS, Laboratoire Modélisation et Simulation Multi Echelle, UMR CNRS 8208, 61 avenue du Général de Gaulle, 94010 Créteil cedex, France

art ic l e i nf o a b s t r a c t

Article history: Dental implants are now widely used for the replacement of missing teeth in fully or partially edentulous
Accepted 24 September 2013 patients and for cranial reconstructions. However, risks of failure, which may have dramatic consequences, are
still experienced and remain difficult to anticipate. The stability of biomaterials inserted in bone tissue depends
Keywords: on multiscale phenomena of biomechanical (bone–implant interlocking) and of biological (mechanotransduc-
Bone tion) natures. The objective of this review is to provide an overview of the biomechanical behavior of the bone–
Implant dental implant interface as a function of its environment by considering in silico, ex vivo and in vivo studies
Osseointegration including animal models as well as clinical studies. The biomechanical determinants of osseointegration
Biomechanical properties phenomena are related to bone remodeling in the vicinity of the implants (adaptation of the bone structure to
Stability
accommodate the presence of a biomaterial). Aspects related to the description of the interface and to its space-
time multiscale nature will first be reviewed. Then, the various approaches used in the literature to measure
implant stability and the bone–implant interface properties in vitro and in vivo will be described. Quantitative
ultrasound methods are promising because they are cheap, non invasive and because of their lower spatial
resolution around the implant compared to other biomechanical approaches.
& 2013 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
2. Description of the bone–implant interface. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
2.1. Geometrical description: bone–implant distance and micromotions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
2.2. Mechanical description: stresses at the interface. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
2.3. Dynamic description: bone remodeling and osseointegration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
3. Implant stability: a space-time multiscale issue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
3.1. Measurement of the multiscale bone properties around the interface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
3.2. Homogenization approaches of bone tissue around the interface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
3.3. Multiscale biomechanical modeling of the bone–implant interface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
4. Implant stability assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
4.1. X-ray and MRI based techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
4.2. Invasive biomechanical methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
4.3. Non invasive biomechanical methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
Conflict of interest statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

n
Corresponding author. Tel.: þ 33 1 45 17 14 41; fax: þ33 1 45 17 14 33.
E-mail address: guillaume.haiat@univ-paris-est.fr (G. Haiat).

0021-9290/$ - see front matter & 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.jbiomech.2013.09.021
4 V. Mathieu et al. / Journal of Biomechanics 47 (2014) 3–13
1. Introduction
Dental implants (see Fig. 1) have been used clinically for more
than thirty years (Albrektsson et al., 2008) and have allowed
considerable progress in dental, oral and maxillofacial surgery, to
restore one or more missing teeth caused by old age or accidents
as well as for esthetic purposes in fully and partially edentulous
patients. Dental implants are also used to support craniofacial
reconstructions and for orthodontic appliances.
Despite their routine clinical use, failures of implant integration
still occur and remain difficult to anticipate. It is difficult to obtain
an accurate estimation of dental implant success ratios due to the
strong and aggressive competition among implant manufacturers
as well as among dental surgeons. Another reason for the difficulty
to assess the implant success ratio lies in its dependence on the
time after surgery considered. A reasonable estimation of dental
implant therapy success ratios is of the order of 75–95% at 10 years
(Karoussis et al., 2004). Predicting dental implant biomechanical
stability is important since implant failures necessitate additional
hazardous painful and expensive surgical interventions.
Despite the aforementioned difficulties, the implants industrial
design has often been driven by an aggressive “copycat” marketing
approach rather than by scientific advances (Brunski, 1999).
Some companies have sometimes copied or made incremental
changes to the sizes, shapes, material and surface properties of
other companies' implants that were deemed to have “worked”.
Clinicians have often used implants in new applications before
research was carried out from a basic science viewpoint. Empirical
approaches may have some advantages but remain limited when it
comes to understand the interaction of the various mechanisms
playing a role in bone healing around an implant.
Two kinds of implant stability should be distinguished. The
primary stability occurs at the moment of implant surgery. It is a
phenomenon of biomechanical nature related to bone quality at
the implant site, which is a necessary condition to obtain the
implant osseointegration. Secondary stability is obtained after a
given healing period and corresponds to the initial stability
reinforced by newly formed bone production and maturation at
10 mm
Fig. 1. Images of three examples of dental implants and their associated abutments: healing abutment for Nobel Biocare© (Kloten, Switzerland) (a), healing and closing
abutments for Implant Diffusion International© (Montreuil, France) (b) and Tekka© (Brignais, France) (c).
the bone–implant interface (Abrahamsson et al., 2004; Berglundh
et al., 2007).
This article reviews various types of works including funda-
mental, animal and clinical studies focusing on the biomechanics
of the bone–dental implant interface but findings obtained in
orthopedic surgery will also be considered since they carry useful
information. The bone–implant interface (which is determinant
for the clinical outcome of the implant (Franchi et al., 2007)) will
first be described in terms of geometrical, mechanical and dyna-
mical properties. Second, the space-time multiscale nature of the
bone–implant interface will be considered, by reviewing the vari-
ous experimental modalities used in vitro as well as the computa-
tional approaches which have been used to retrieve information
on the interface. Eventually, the various methods used to assess
the implant stability will be described. Note that purely biochem-
ical or biological factors (Kerner et al., 2009; Michiardi et al., 2010)
are out of scope of this review, focusing on biomechanical aspects
which are still poorly understood. Although the importance of the
mechanical strength (quasi-static situation) and of the stiffness
degradation and endurance limit (which is assessed by fatigue
tests) of the implant materials has been evidenced (Lee et al.,
2009), the present paper is dedicated to bone biomechanics
rather than to the implant material itself. The effects of implant
surface (Taborelli et al., 1997), of surface functionalization (Junker
et al., 2009), of implant geometry (Quaresma et al., 2008) and of
biocompatibility as well as factors related to the patients are not
considered in this study.
2. Description of the bone–implant interface
The biomechanical properties of the bone–implant interface
are the key determinants for the implant stability as well as for the
evolution of the implant status. The bone–implant interface
properties are determined by the quantity of the implant surface
in intimate contact with mineralized bone tissue as well as by
the mechanical quality of bone tissue around the interface. From
the biomechanical point of view, the difficulty comes from the fact
 V. Mathieu et al. / Journal of Biomechanics 47 (2014) 3–13
the interface has a complex nature due to (i) its roughness, (ii) the
fact that bone is in partial contact with the implant, (iii) adhesion
phenomena between bone and the implant and (iv) the time-
evolving nature of the interface properties. The problem consid-
ered can therefore be treated from various complementary points
of view: by considering the interface geometry (bone–implant
distance), the static mechanical phenomena (stresses at the
interface) or from a dynamic (time evolving) point of view, thus
considering remodeling phenomena of bone tissue around the
interface.
2.1. Geometrical description: bone–implant distance and
micromotions
When an intimate surgical fit between bone and the implant
surface occurs after surgery, the interfacial bone undergoes remo-
deling and is gradually substituted with mature lamellar bone.
However, when a healing chamber forms in regions where bone
and implants are not in intimate contact, rapid woven bone filling
occurs and long term implant stability is ensured by bone model-
ing and remodeling processes. When primary stability is not
sufficient, micro-movements may appear preventing good healing
conditions and leading to the formation of fibrous tissue and to
surgical failure (Heller and Heller, 1996; Rangert et al., 1997).
Animal studies conducted in orthopedic surgery have suggested
that relative micromotion between the implant and bone tissue
should not exceed about 150 mm, above which fibrous tissue rather
than bone ingrowth dominates (Pilliar et al., 1986; Søballe et al.,
1992). Dental implant studies have shown that during bone
healing, micromotions at a relatively low level may be responsible
for biomechanical stimulation of bone remodeling. However,
fibrous tissue may develop instead of an osseointegrated interface
when there is excessive interfacial micromotion early after surgery
(Duyck et al., 2006; Orlik et al., 2003). The critical parameter is not
the absence of loading, but the absence of excessive micromotion
at the bone–implant interface (Szmukler-Moncler et al., 2000).
However, the precise determination of the evolution of the
micromotion threshold (above which fibrous tissues develop) as
a function of healing time remains to be investigated.
2.2. Mechanical description: stresses at the interface
When functional loading exerted via the implant exceeds
“a certain stress s0”, the implant is regarded as being “overloaded”,
leading to possible complications such as peri-implant bone resorp-
tion. However, stresses below s0 are beneficial for the implant
outcome and stimulate bone remodeling phenomena. The determi-
nation of the value of s0 remains unclear (Zhang et al., 2012b)
because (i) it is difficult to obtain a controlled stress field in vivo, (ii)
the value of s0 depends on various factors such as bone remodeling
properties, healing time (s0 is expected to increase as a function of
healing time) or osseointegration and (iii) the value of s0 depends on
the nature of the stress considered (shear or compression) as well as
of the direction (bone being an anisotropic medium at all scales).
Optimal loading conditions history strongly depends on the patient
and on the ability of bone tissue to adapt its structure to its
environment through remodeling phenomena (Albrektsson et al.,
1981). An appropriate balance between reasonable initial stresses
and a good primary stability is the key determinant for the long term
success of the implant stability (Lioubavina-Hack et al., 2006). Note
that the cortical bone–implant interface is the most important region
regarding the implant success due to highest bone stresses occurring
in cortical bone around the implant neck (Sutpideler et al., 2004).
5
2.3. Dynamic description: bone remodeling and osseointegration
Implant osseointegration, a phenomenon discovered by Bråne-
mark, consists in the time evolution of bone structure to obtain a
direct, structural and functional connection between living bone
and the loaded implant surface (Sykaras et al., 2000; Wenz et al.,
2008). An implant is osseointegrated when newly formed bone
tissue is in intimate contact with the implant surface so that at the
microscopic level, no interposition of fibrous tissue occurs.
Assessing the efficiency of osseointegration phenomena is a
difficult problem because it requires the local (around the inter-
face) measurement of the biomechanical properties of bone tissue,
which has a complex nature with viscoelastic, anisotropic and
heterogeneous properties. Moreover, bone tissue adapts its struc-
ture to mechanical stresses through remodeling phenomena
(Wolff, 1892). Bone regeneration under implants lasts several
months during which the temporal evolution and spatial distribu-
tion of the bone properties are strongly heterogeneous. Osteoblast
cells rule the main steps of bone regeneration (Goto et al., 2004):
(i) deposition of extracellular matrix (ECM), an unmineralized
collagen-rich tissue, (ii) production of the hormones responsible
for the mineralization of the ECM with calcium and phosphates
ions to form woven bone and (iii) remodeling of woven bone to
mature bone. The process of bone formation is affected by local
features (fluid and chemical pathways and stress state) (Swan
et al., 2003). It is generally assumed that osteoclastic activity
undermines primary stability before new bone formation prevents
implant micromotion. Note that bone remodeling related issues
constitute a highly active field of research which is not detailed in
the present paper.
The effect of mechanical loading on bone adaptation primarily
applies to tissue located around the implant (Duyck et al., 2007;
Duyck et al., 2006; Isidor, 2006). Force or displacement controlled
mechanical loading at low-frequency ( o10 Hz) improves bone
formation around the implant. High-frequency whole body load-
ing ( 410 Hz) can also lead to increased bone formation in the
peri-implant surroundings and to an improved osseointegration
(Akca et al., 2007; Ogawa et al., 2011a; Ogawa et al., 2011b). The
optimal loading parameters have been determined (Zhang et al.,
2012a; Zhang et al., 2012b) in terms of frequency and amplitude to
enhance osseointegration. At much higher frequency, Low Inten-
sity Pulsed UltraSound (LIPUS), which has widely been used to
enhance bone fracture healing in the context of orthopedic surgery
(Harle et al., 2001; Heybeli et al., 2002; Tsai et al., 1992; Wang
Secondary stability
Trabeculae,
Hydroxyapatite Collagen fibers Loading
osteons
procedure
Implant Material
Time
Surface treatment, Micro motions,
roughness stresses Anatomy
Primary stability
Temperature increase Surgical
Asepsis Implant design
during drilling protocole
50 nm 5 µm 500 µm 5 mm
Space
Fig. 2. Diagram representing the multi-scale and multi-time natures of the
different phenomena occurring during osseointegration of a dental implant. Three
groups of factors are considered: the factors relative to implants properties (dashed
line), to the surgeon (dotted line) and the ones related to bone properties (solid
lines).
6 V. Mathieu et al. / Journal of Biomechanics 47 (2014) 3–13
et al., 1994; Yang et al., 1996), has also been employed recently
to stimulate dental implant osseointegration (Hsu et al., 2011;
Liu et al., 2012; Ustun et al., 2008).
The various points of view considered in this section highlight
the complex nature of the bone–implant interface. Another
difficulty lies in its multiscale nature illustrated in Fig. 2 which
shows a space-time diagram representing the various biomecha-
nical factors influencing implant stability. Three groups of factors
are considered: the factors relative to implants properties (dashed
line), to the surgeon intervention (dotted line) and the ones
related to bone properties (solid lines).
3. Implant stability: a space-time multiscale issue
As shown in the previous section and in Fig. 2, the phenomena
occurring at the bone–implant interface and involving load trans-
fers between bone and the implant are of space-time multiscale
nature. Note that as illustrated in Fig. 2, implant design at the scale
of the millimeter (self tapping or not (Markovic et al., 2013),
implant length (Hong et al., 2012), implant shape (Wu et al., 2012),
abutment (Balik et al., 2012), thread pitch (Orsini et al., 2012))
plays an important role in implant stability (particularly for
primary stability) and in stress distribution at the implant inter-
face. At the scale of the implant (several millimeters), load is
transferred via macroscopic stress distribution. At the scale of
around 50 mm, the roughness plays a role in stimulating the
growth of newly formed bone tissue (Shalabi et al., 2007). At the
scale of around 100 nm, biochemical factors become important
through adhesion phenomena between bone and implant sur-
faces. Moreover, the temporal multiscale nature of the problem
comes from the fact that the time constant of the implant
mechanical solicitation (typically around the second) is several
orders of magnitude lower than the time constant of bone
structure modifications (around several weeks). To understand
this space-time multiscale issue, various complementary appro-
aches need to be carried out. Bone tissue biomechanical properties
have been measured around the implant but purely experimental
approaches remain limited when it comes to understand the
interaction between the different spatial and temporal constants.
Therefore, homogenization techniques have been developed to
climb the hierarchy of scales in newly formed bone tissue, from
the nanoscale up to the macroscopic level (Sansalone et al., 2010).
Computational approaches are necessary to assess the bone
mechanical behavior on the basis of its internal structure and are
complementary with experimental measurements since they use
the experimental results as input data in the models.
100 µm 7 weeks
Fig. 3. Histological images of two fragments of bone–implant interfaces for 7 weeks (a) and 13 weeks (b) healing time. The limit between pre existing mature bone tissue
and newly formed bone tissue is represented with white dotted lines.
3.1. Measurement of the multiscale bone properties
around the interface
The biomechanical properties of bone tissue at a distance lower
than around 100–200 mm from the implant surface are the critical
parameters determining implant stability (Huja et al., 1999; Luo
et al., 1999). Various experimental approaches may be used to
retrieve complementary information on newly formed bone prop-
erties at the scale of around several micrometers. Such informa-
tion may then be used as input data in the modeling of the
mechanical behavior of bone tissue in the vicinity of the implant
(see Section 3.2) and then at the scale of the implant.
(i) Histology
The gold standard for the assessment of the implant osseointe-
gration is given by histological measurements, which are realized
by embedding the samples in Methacrylate-based resin, cutting
them in 100 mm thick slices (Bernhardt et al., 2012; Nkenke et al.,
2003; Singhrao et al., 2012), and staining them (Artzi et al., 2003a,
2003b; Mathieu et al., 2011a). The visualization of the slides
allows measuring the bone implant contact fraction (BIC). Color-
ing agents enable to obtain a qualitative estimation of the degree
of mineralization of bone tissue around the implant (dark colors
corresponding to more mineralized regions). Histological analysis
enables (i) to distinguish mature pre-existing from newly-formed
bone tissue (white dashed lines in Fig. 3), (ii) to measure a
significant increase of BIC as a function of healing time and (iii) to
obtain a qualitative estimation of the increase of mineralization of
newly formed bone tissue. The key feature of quantitative bone–
implant histology is the undecalcified embedding of the sample
blocks without removing the implant. This was a breakthrough in
the 1990's in comparison with conventional microtomy based
histology, where implants had to be removed and bone samples
to be decalcified, causing loss of interface information. However,
histology does not provide quantitative information on the
biomechanical properties of newly bone tissue.
(ii) Small angle X-ray scattering (SAXS)
SAXS is used to assess the thickness, orientation and shape/
arrangement of the mineral crystals in bone tissue. SAXS
measurements have been carried out near the implant surface
(Bunger et al., 2006) and showed that (i) the mineral crystals
tended to be aligned with the surface of the implants and (ii)
the mineral crystal thickness increased linearly with distance
from the implant. However, SAXS does not allow to retrieve
directly any mechanical properties.
(iii) Nanoindentation
Nanoindentation is a technique widely used to investigate
the biomechanical properties of different materials at the
13 weeks
 V. Mathieu et al. / Journal of Biomechanics 47 (2014) 3–13
microscopic scale (Zysset et al., 1999) yielding information on
the apparent Young's modulus and on the hardness. Nanoin-
dentation has been used to show that Young's modulus and
hardness values are lower in the vicinity of the implant than
in mature bone (Chang et al., 2003; Seong et al., 2009).
(iv) Scanning Acoustic Microscopy (SAM)
SAM (Meunier et al., 1988) is another technique allowing the
measurement of an image of the acoustic impedance (given
by the product of tissue mass density and ultrasonic velocity)
at the scale of several micrometers. SAM was used for the
qualitative assessment of the biomechanical microstructural
properties of the bone–implant interface with a resolution of
a few micrometers (Nomura et al., 2006).
(v) Micro Brillouin scattering
Micro Brillouin scattering technique uses the photo acoustic
interaction between a laser beam and a sample to measure
bone speed of sound with a resolution of a few micrometers.
Using an animal model derived and adapted from (Rønold and
Ellingsen, 2002b; Rønold et al., 2003a; Rønold et al., 2003b,
2003c), a “bone chamber” exclusively containing newly
formed bone tissue (see Fig. 4) was used to measure the
biomechanical properties of newly formed bone tissue with a
multimodal experimental approach coupling nanoindentation
(Vayron et al., 2011; Vayron et al., 2012), micro Brillouin
scattering (Mathieu et al., 2011a) and histology. Histological
analysis was carried out after different healing times (see
Fig. 3). As shown in Table 1, lower ultrasonic velocity, Young's
modulus and hardness values were obtained in newly formed
bone tissue compared to mature bone, which might be
explained by the lower mineral content. The coupling of
nanoindentation with micro Brillouin analysis is a powerful
approach because measurements are realized at the same
scale (a few micrometers), allowing to retrieve the relative
variation of mass density between newly formed and mature
Fig. 4. Schematic representation of the coin-shaped implant model.
Table 1
Mean values and standard deviation of the indentation modulus and hardness measured by nanoindentation and of the ultrasound velocity measured with micro Brillouin
scattering in newly formed (7 weeks) and mature bone tissue of New Zealand White Rabbits. Data taken from (Vayron et al., 2011; Vayron et al., 2012; Mathieu et al., 2011a).
The relatively low standard deviation may be explained by (i) the low number of measurements (only one implant was considered) and (ii) the combined use of histology
and of the dedicated animal model, which allows to distinguish newly formed bone and mature bone tissue and to realize the measurements in each medium independently.
Quantity (averaged values) Newly formed bone tissue
Young's modulus (GPa) 15.85 ( 71.55)
Hardness (GPa) 0.66 ( 70.1)
Ultrasound velocity (m/s) 4970 ( 7140)
7
bone tissues, which is of the order of 13.5% (Vayron et al.,
2012).
The main challenge when employing experimental measure-
ments to assess newly formed bone properties around the implant
lies in the decrease of the resolution. Scale reduction is a critical
point in order to be able to use accurate input data in the
multiscale model of bone mechanical properties described below.
3.2. Homogenization approaches of bone tissue around the interface
Recent studies pursued the idea to climb the hierarchy of
scales, from the nanoscale up to the macroscopic level. A key
point lies in the identification of building blocks at the micro-
scopic- and nanoscopic-level which could explain bone elasticity
at the macroscopic scale. At the organ level, models are often
continuum based (Ilic et al., 2010) and describe the variation of
bone apparent density as a function of the biological and mechan-
ical stimuli. At the tissue level, models account for the bone
microarchitecture and remodeling properties. At the cellular level,
cellular interactions are analyzed in the temporal domain and
molecular dynamics approaches are employed to obtain the
elastic properties (Izaguirre et al., 2004; Vesentini et al., 2005).
In addition to modulating cell adaptation, mechanochemical
signals also influence proliferation, migration and differentiation
(Knothe Tate, 2011; Knothe Tate et al., 2008). Although informa-
tive, most models are usually developed independently of each
other and their interpretation is therefore limited.
Continuum micromechanic approaches allow the modeling of
bone anisotropic elastic behavior (Hellmich et al., 2008). Models
should also account for the flow channels (Sansalone et al., 2012)
which provide conduits for fluid flow, enhancing molecular and
cellular transport and inducing shear stresses via fluid drag at the
cell surfaces. Micromechanical models have considered micro-
structural features, such as osteonal fibers embedded in a matrix
of interstitial bone (Dong and Guo, 2006).
Coupling 3-D high-resolution reconstructions with numerical
simulation tools (Haiat et al., 2009) has become a common
approach to retrieve the bone mechanical properties because of
the difficulty of achieving reliable estimations of stress and strain
fields in vivo. However, a critical issue consists in the aniso-
tropy and heterogeneity of bone tissue. When heterogeneity is
accounted for, empirical regression analyses between tissue
mineral density and Young's modulus have often been employed
(Keyak and Falkinstein, 2003; Yosibash et al., 2007). An homo-
genization model was developed to infer the nanoscale up to the
organ scale using data obtained from synchrotron radiation
micro computed tomography (mCT) (Sansalone et al., 2012;
Sansalone et al., 2010). However, the existing multiscale models
(for instance accounting for the effect of angiogenesis (Checa
and Prendergast, 2009), fluid flow (Geris et al., 2004) and blood
clotting (Vanegas-Acosta et al., 2011)) do not account for the
Mature bone tissue Number of measurements
New bone: 106
20.66 ( 72.75)
Mature bone: 132
New bone: 106
0.696 ( 70.15)
Mature bone: 132
New bone: 6
5310 ( 740)
Mature bone: 6
8 V. Mathieu et al. / Journal of Biomechanics 47 (2014) 3–13
temporal bone evolution as well as for the full interaction between
the nanoscale and the organ scale, which prevents one from
understanding aspects related to bone regulation and regenera-
tion. Many challenges have to be faced including the need for a
model providing a reliable movie of the system evolution.
3.3. Multiscale biomechanical modeling of the
bone–implant interface
Various approaches have been developed to model the mechan-
ical behavior of the bone–implant interface. The biological threshold
for micro-movements being in the range 100–200 mm, the difficulty
lies in that the accuracy must be lower than 10–20 mm or better.
Finite element methods (FEM) have been widely employed to
simulate the mechanical behavior of an implant at the organ scale
using large sliding contact elements in the case of primary stability
(Bernakiewicz and Viceconti, 2002; Lin et al., 2006; Viceconti et al.,
2000). Frictional Coulomb law has been employed (Andreaus and
Colloca, 2009), some methods using empirical remodeling laws
(Folgado et al., 2009; Perez et al., 2008; Rungsiyakull et al., 2010),
non linear anisotropic FEM (Simon et al., 2003) or coupling of FEM
with statistical techniques (Laz et al., 2006; Viceconti et al., 2006;
Younesi et al., 2010) to account for the uncertainty related to the
in vivo situation. However, the existing approaches to model bone–
implant interfaces do not account for the multiscale and evolving
nature of bone tissue. The biomechanical modeling of the bone–
implant interface often remains simplistic, due to a lack of experi-
mental data at the scale of 1–100 mm and the main challenge consists
in accounting for the heterogeneity of bone biomechanical properties
around the implant at the micrometer scale (described in Sections
3.1 and 3.2) on the implant mechanical behavior.
4. Implant stability assessment
Basic scientists as well as clinical investigators have attempted
to decrease treatment time frames by reducing the healing period.
To do so, assessing the implant stability is of critical importance to
adapt surgical strategies to the various factors affecting implant
stability (see Fig. 2).
4.1. X-ray and MRI based techniques
The resolution of clinical X-ray based techniques (such as
radiography or mCT) around the implant interface is limited due
to X-ray metal artifacts related to the presence of metallic
components in the constitution of the large majority of dental
implants (Shalabi et al., 2007). Similarly, the use of magnetic
resonance imaging (MRI) (Potter et al., 2004) has been proposed
but remains of limited interest due to magnetic fields disturbance
(Gill and Shellock, 2012; Hecht et al., 2011; Knothe Tate et al.,
2008). X-ray or MRI based techniques can give access to informa-
tion on bone microstructure and tissue mineral density which
have a strong influence on the mechanical properties of bone
tissue (Hsu et al., 2013a). However, the estimation of bone
microstructure and tissue mineral density is not sufficient for
the direct characterization of bone mechanical properties since
material properties at the microscale are also important. As a
consequence, X-ray or MRI based techniques are not commonly
used in order to assess the biomechanical properties of the bone–
implant interface. For these reasons, biomechanical methods have
been developed.
4.2. Invasive biomechanical methods
Numerous animal studies have focused on the mechanical
stability of implants but these studies often remain of limited interest
to understand the basic phenomena responsible for implant stability
because they use real implants with complex geometrical configura-
tions, which does not allow (i) to carry out biomechanical testing
under controlled conditions and (ii) to retrieve quantitative informa-
tion on the adhesion of the bone–implant interface.
For these reasons, specific implant models with a planar bone–
implant interface have been conceived to minimize the effects
of friction and of mechanical forces introduced by surface rough-
ness and to work under standardized conditions (Skripitz and
Aspenberg, 1998). Rønold et al. (Rønold and Ellingsen, 2002a) have
carried out nice systematic studies aiming at establishing a model
for testing functional attachment of implants in situ. Their pull-out
model makes it possible to study the relation between kinematics
and strength of bone bonding with negligible influence of shear
forces or mechanical interlocking. The systematic approach of
Rønold et al. is promising but remains in some regards limited
when it comes to the analysis of the phenomena involved in the
rupture between bone and the implant. From an adhesive contact
mechanics point of view, the tensile test performed corresponds to
a flat-punch configuration (see Fig. 5a), which is a mechanically
unstable situation (Maugis, 2000). Therefore, the measured pull-
out force strongly depends on initial and boundary conditions and
cannot be used to retrieve the adhesion energy, which is the only
physically meaningful parameter. For these reasons, an experi-
mental approach based on a mode III cleavage mechanical device
aiming at understanding the behavior of a planar bone–implant
interface submitted to torsional loading was developed (see
Fig. 5b) (Mathieu et al., 2012b). Coin-shaped titanium implants
(see Fig. 4) were inserted on the tibiae of a New Zealand White
rabbit for seven weeks. After sacrifice, mode III cleavage experi-
ments were performed on bone samples. An analytical model
allowed to assess the values of different parameters related to
bone tissue at the vicinity of the implant. The approach allows to
estimate different physical quantities related to the bone–implant
interface such as: torsional stiffness (around 20.5 N m rad  1),
bone shear modulus (around 240 MPa), maximal torsional loading
(around 0.056 N m), mode III fracture energy (around 77.5 N m  1)
and the associated stress intensity factor (0.27 MPa m1/2).
4.3. Non invasive biomechanical methods
(i) Empirical approaches
Surgeons commonly use empirical tests to estimate the
primary stability of dental implants. The most widely used
approach consists in hitting the implant with a stick and
listening to the noise produced by the system. Another
approach consists in measuring the insertion torque during
the surgical procedure. However, these methods remain
highly empirical and do not allow assessing the biomechani-
cal properties of the bone–implant interface.
(ii) Impact based approaches
The PerioTests device (Schulte et al., 1983) has been on the
market since the 80's. Initially, it was dedicated to the
evaluation of tooth mobility in the context of parodontopa-
thies. Then, its use has been extended to assess dental implant
stability. The device comprises a hand piece which is posi-
tioned perpendicularly to the implant axis. A metallic rod hits
the implant and the contact duration is recorded, leading to a
PerioTest value (PTVs). However, the criteria for evaluating
natural tooth mobility are different from those used to assess
implant mobility because the supporting mechanism of den-
tal implant is different from that of a natural tooth.
 V. Mathieu et al. / Journal of Biomechanics 47 (2014) 3–13
Implant
Bone tissue
Fig. 5. Schematic representation of two configurations of mechanical loadings for the rupture of the bone–implant interface using coin shaped implants.
A correlation between PTV values and (i) implant mobility
and (ii) the level of marginal bone (Chai et al., 1993; Haas
et al., 1999; Nkenke et al., 2003) has been shown but PTV
values depend on the anatomical location of the implant
(Salonen et al., 1997; Tricio et al., 1995; Vansteenberghe et al.,
1995). Numerous studies have shown that PTV values
decrease as a function of healing time, when bone density
increases around the implant. However, no correlation
was found between PTV and the bone implant contact (BIC)
using histomorphometric analyses (Caulier et al., 1997;
Mericskestern et al., 1995; Nkenke et al., 2003), which indi-
cates that the Periotest method is sensitive to variations of the
surrounding bone properties but not to the bone–implant
interface properties. PTV measurements are strongly influ-
enced by the position of the impact location and by the angle
of the device relatively to the implant axis (Derhami et al.,
1995). Therefore, it remains difficult to use the Periotest
for monitoring purposes due to reproducibility and precision
error related issues.
(iii) Resonance frequency analysis
In the field of structural integrity monitoring, the analysis of
the frequency response of mechanical structures to dynamic
loads has been widely investigated for decades (Adams et al.,
1978). The frequency response has been used as a diagnostic
parameter in structural assessment procedures using vibra-
tion monitoring: natural frequencies are sensitive indicators
of structural integrity and relationships between frequency
changes and structural damage have been evidenced (Salawu,
1997).
In the 90's, the technique of resonance frequency analysis
(RFA) was transposed to the field of implant stability diag-
nosis (Meredith et al., 1996). It consists in the measurement of
the first resonance frequency of the bone–implant system.
A L-shaped transducer is screwed into the implant and is
excited at various frequencies (from 5 to 15 kHz). The first
resonance frequency is used as an indicator of the implant
stability through an index called Implant Stability Quotient
(ISQs). The system is commercialized under the name
Osstell™ (Integration Diagnostics Ltd., Göteborgsvägen, Swe-
den). The latest version of the RFA device uses a “Smartpeg”
(Herrero-Climent et al., 2012), which is a piece screwed into
the implant abutment. The “Smartpeg” is excited mechani-
cally in a non contact mode using a hand-held probe and
allowing to increase measurement accuracy in a clinical
context (Geckili et al., 2012; Hsu et al., 2013b; Oh and Kim,
2012).
The main interest of the ISQ score in a clinical context is that it
allows quantification tool for clinicians (Park et al., 2012). The
9
Implant
Bone tissue
RFA technique is sensitive to the rigidity of the implant and of
the surrounding bone. An increase of ISQ values has been
evidenced as a function of healing time, which has been
explained by bone formation around the implant. A correla-
tion has been shown between the initial ISQ value and (i) the
cutting torque (Friberg et al., 1999) and (ii) bone density
measurements assessed empirically by the surgeon before
implantation (Alsaadi et al., 2007). A correlation between
cortical bone thickness and the ISQ value has also been
established (Nkenke et al., 2003; Sennerby et al., 2005).
A relationship between ISQ values and the anatomical region
of implantation has been evidenced (Balleri et al., 2002;
Barewal et al., 2003; Bischof et al., 2004; Ostman et al., 2006).
However, various limitations have been mentioned in the
literature. The “fundamental flaw” in the Osstell device is that
it reduces the dynamic response of the bone–implant system
to the first resonance frequency and tries to capture this in an
‘ISQ’ value, which is intuitively easy for the clinician but has
only limited value from a structural mechanics point of view.
ISQ may be seen as an “oversimplification” of the frequency
response of the bone–implant system. The correlation
between ISQ values and marginal bone level is only obtained
during the first six months after surgery (Turkyilmaz, 2006).
At early times after surgery, a decrease of stability may occur
(Balshi et al., 2005; Coelho et al., 2010; Glauser et al., 2004;
Huwiler et al., 2007; Raghavendra et al., 2005). However, it is
not clear whether the decrease of ISQ values during the first
several weeks is exclusively related to marginal bone loss
since other reasons such as bone relaxation following the
compression of bone tissue during the implant insertion may
also play a role (Barewal et al., 2003; Glauser et al., 2003;
Glauser et al., 2004; Huwiler et al., 2007). The sensitivity of
the ISQ value to the implant stability depends on the implant
type (Nedir et al., 2004a). The clear cut relationship between
ISQ values and the percentage of bone in contact with the
implant remains unclear (Scarano et al., 2006; Seong et al.,
2009).
The rigidity of the entire bone–implant system measured
with the RFA device depends on the biomechanical properties
of the implant, of the bone–implant interface and of the
surrounding bone tissue. Therefore, the first resonance fre-
quency is not only related to bone–implant interface proper-
ties but rather to the bone properties at the scale of the
organ (Aparicio et al., 2006). Meanwhile, bone properties at
the scale of around 50–200 mm are the critical properties
determining the implant osseointegration (Winter et al.,
2004). Moreover, the fixation and the orientation of the
transducer influence significantly the measured ISQ values,
10 V. Mathieu et al. / Journal of Biomechanics 47 (2014) 3–13
thus rendering its clinical use difficult (Pattijn et al., 2007).
Diagnostic criteria for the failure of the implantation have
not been established (Atsumi et al., 2007). Despite the
aforementioned limitations, RFA is still being used in many
clinical studies to quantify implant stability (Nedir et al.,
2004b; Rabel et al., 2007; Turkyilmaz et al., 2007;
Valderrama et al., 2007).
(iv) Quantitative ultrasound methods
Quantitative ultrasound (QUS) techniques are now routinely
used clinically to assess bone fragility (Laugier and Haiat, 2011).
In dentistry, QUS is mostly used to measure enamel thickness
(Ghorayeb et al., 2008) and periodontal pocket depth (Lynch
and Hinders, 2002; Palou et al., 1987). The main interest of QUS
is that it is non invasive, it is relatively cheap and that it does
not involve ionizing radiation. Moreover, ultrasound being
mechanical waves, it is adapted to retrieve the biomechanical
properties of living tissues. Storani et al. (Storani de Almeida
et al., 2007) performed experiments with a screw inserted in
an aluminum block and measured the variations of its ultra-
sonic response. This technique was adapted by investigating
the potentiality of QUS to assess the amount of bone in contact
with titanium prototype cylindrical implants. The 10 MHz
ultrasonic response of the implant was processed to derive a
quantitative indicator I, based on the temporal variation of the
signal amplitude (Mathieu et al., 2011c). The results revealed a
statistical distribution of I significantly correlated with the
amount of bone in contact with the cylinders. Moreover, 2-D
finite difference time domain simulations were performed
(Mathieu et al., 2011b) to understand the propagation phe-
nomena of ultrasonic waves in the prototype cylindrically
shaped implants. The ultrasonic response is influenced by
(i) the amount of bone in contact with the implant, (ii) cortical
bone thickness, and (iii) surrounding bone material properties.
The approach was applied to real dental implants used in the
clinic which were embedded in a biomaterial used as bone
substitute material and subject to fatigue loading (Vayron et al.,
2013). The indicator I was shown to be sensitive to the fatigue
time. Moreover, the same approach was carried out to show
that the ultrasound response of an implant varies as a function
of bone primary stability (Vayron et al., Haïat, submitted for
publication). Recently, several studies have shown the potential
of non linear ultrasound techniques to study the stability of
dental implants (Riviere et al., 2010; Riviere et al., 2012a;
Riviere et al., 2012b). All these studies show the potentiality
of QUS methods to assess the quality of bone tissue in contact
with the implants, opening new paths to (i) investigate the
material properties around a dental implant and (ii) optimize
the conception of bone substitute materials in the context of
dental implant surgery.
The coin-shaped implants described in (Section 3.1) were also
used to investigate the effect of bone healing on the ultrasonic
response of the bone–implant interface. The ultrasound
response of the interface was measured in vitro at 15 MHz
after seven and thirteen weeks of healing time (Mathieu et al.,
2012a). The bone–implant contact was measured by histomor-
phometry and the degree of mineralization of bone was
estimated qualitatively by histological staining. The significant
decrease of the amplitude of the echo of the bone–implant
interface as a function of healing time is explained by (i) the
increase of the BIC (from 27% to 69%) and (ii) the increase of
mineralization of newly formed bone tissue.
All these studies show the potentiality of QUS techniques to
investigate bone quality around the implant. However, further
work is necessary in order to improve the reproducibility of the
measurements and to consider real implants used in the
clinics.
5. Conclusion
Assessing primary and secondary dental implant stability is
a complex problem due to the multiscale and time dependent
nature of newly formed bone tissue around implants. While
multiscale models have been developed to bridge the nanoscale
up to the organ scale, the main difficulty now lies in introducing
remodeling phenomena within these models in order to under-
stand the evolution of dental implant stability. The evolution of
newly formed bone properties around implants is the determinant
factor in order to predict the clinical outcome of dental implants.
Different invasive methods have been developed in the laboratory
in order to measure in vitro newly formed bone tissue, but most of
them remain difficult to be employed in vivo. X-ray or MRI based
techniques are not adapted to an in vivo use due to resolution
issues at the bone–implant interface. Therefore, various biome-
chanical methods have been developed in order to overcome this
limitation but most of them are limited when it comes to analyze
the biomechanical properties of newly formed bone tissue. Quan-
titative ultrasound methods are promising because they are cheap,
non invasive and because of their higher spatial resolution around
the implant compared to other biomechanical approaches.
Conflict of interest statement
There is no conflict of interest of any kind.
Acknowledgments
This work has been supported by French National Research
Agency (ANR) through EMERGENCE program (project WaveIm-
plant no. ANR-11-EMMA-039).
References
Abrahamsson, I., Berglundh, T., Linder, E., Lang, N.P., Lindhe, J., 2004. Early bone
formation adjacent to rough and turned endosseous implant surfaces. An
experimental study in the dog. Clinical Oral Implants Research 15, 381–392.
Adams, R.D., Cawley, P., Pye, C.J., Stone, B.J., 1978. A vibration technique for non-
destructively assessing the integrity of structures. Journal of Mechanical
Engineering Science 20, 93–100.
Akca, K., Sarac, E., Baysal, U., Fanuscu, M., Chang, T.L., Cehreli, M., 2007. Micro-
morphologic changes around biophysically-stimulated titanium implants in
ovariectomized rats. Head and Face Medicine 3, 28.
Albrektsson, T., Branemark, P.I., Hansson, H.A., Lindstrom, J., 1981. Osseointegrated
titanium implants. Requirements for ensuring a long-lasting, direct bone-to-
implant anchorage in man. Acta Orthopaedica Scandinavica 52, 155–170.
Albrektsson, T., Sennerby, L., Wennerberg, A., 2008. State of the art of oral implants.
Periodontology 2000 (47), 15–26.
Alsaadi, G., Quirynen, M., Michiels, K., Jacobs, R., van Steenberghe, D., 2007. A
biomechanical assessment of the relation between the oral implant stability at
insertion and subjective bone quality assessment. Journal of Clinical Period-
ontology 34, 359–366.
Andreaus, U., Colloca, M., 2009. Prediction of micromotion initiation of an
implanted femur under physiological loads and constraints using the finite
element method. Proceedings of the Institution of Mechanical Engineers Part H
– Journal of Engineering in Medicine 223, 589–605.
Aparicio, C., Lang, N.P., Rangert, B., 2006. Validity and clinical significance of
biomechanical testing of implant/bone interface. Clinical Oral Implants
Research 17, 2–7.
Artzi, Z., Givol, N., Rohrer, M.D., Nemcovsky, C.E., Prasad, H.S., Tal, H., 2003a.
Qualitative and quantitative expression of bovine bone mineral in experimental
bone defects. Part 1: description of a dog model and histological observations.
Journal of Periodontology 74, 1143–1152.
Artzi, Z., Givol, N., Rohrer, M.D., Nemcovsky, C.E., Prasad, H.S., Tal, H., 2003b.
Qualitative and quantitative expression of bovine bone mineral in experimental
bone defects. Part 2: morphometric analysis. Journal of Periodontology 74,
1153–1160.
Atsumi, M., Park, S.H., Wang, H.L., 2007. Methods used to assess implant stability:
current status. International Journal of Oral and Maxillofacial Implants 22,
743–754.
Balik, A., Karatas, M.O., Keskin, H., 2012. Effects of different abutment connec-
tion designs on the stress distribution around five different implants:
 V. Mathieu et al. / Journal of Biomechanics 47 (2014) 3–13
A 3-dimensional finite element analysis. Journal of Oral Implantology 38,
491–496.
Balleri, P., Cozzolino, A., Ghelli, L., Momicchioli, G., Varriale, A., 2002. Stability
measurements of osseointegrated implants using Osstell in partially edentulous
jaws after 1 year of loading: a pilot study. Clinical Implant Dentistry and
Related Research 4, 128–132.
Balshi, S.F., Allen, F.D., Wolfinger, G.J., Balshi, T.J., 2005. A resonance frequency
analysis assessment of maxillary and mandibular immediately loaded implants.
International Journal of Oral and Maxillofacial Implants 20, 584–594.
Barewal, R.M., Oates, T.W., Meredith, N., Cochran, D.L., 2003. Resonance frequency
measurement of implant stability in vivo on implants with a sandblasted and
acid-etched surface. International Journal of Oral and Maxillofacial Implants 18,
641–651.
Berglundh, T., Abrahamsson, I., Albouy, J.P., Lindhe, J., 2007. Bone healing at
implants with a fluoride-modified surface: an experimental study in dogs.
Clinical Oral Implants Research 18, 147–152.
Bernakiewicz, M., Viceconti, M., 2002. The role of parameter identification in finite
element contact analyses with reference to orthopaedic biomechanics applica-
tions. Journal of Biomechanics 35, 61–67.
Bernhardt, R., Kuhlisch, E., Schulz, M.C., Eckelt, U., Stadlinger, B., 2012. Comparison
of bone–implant contact and bone–implant volume between 2D-histological
sections and 3D-SR mu CT slices. European Cells and Materials 23, 237–248.
Bischof, M., Nedir, R., Szmukler-Moncler, S., Bernard, J.P., Samson, J., 2004. Implant
stability measurement of delayed and immediately loaded implants during
healing. A clinical resonance-frequency analysis study with sandblasted-and-
etched ITI implants. Clinical Oral Implants Research 15, 529–539.
Brunski, J.B., 1999. In vivo bone response to biomechanical loading at the bone/
dental-implant interface. Advances in Dental Research 13, 99–119.
Bunger, M.H., Foss, M., Erlacher, K., Li, H., Zou, X., Langdahl, B.L., Bunger, C., Birkedal, H.,
Besenbacher, F., Pedersen, J.S., 2006. Bone nanostructure near titanium and porous
tantalum implants studied by scanning small angle X-ray scattering. European
Cells and Materials 12, 81–91.
Caulier, H., Naert, I., Kalk, W., Jansen, J.A., 1997. The relationship of some histologic
parameters, radiographic evaluations, and Periotest measurements of oral
implants: an experimental animal study. International Journal of Oral and
Maxillofacial Implants 12, 380–386.
Chai, J.Y., Yamada, J., Pang, I.C., 1993. In vitro consistency of the Periotest instrument.
Journal of Prosthodontics 2, 9–12.
Chang, M.C., Ko, C.C., Liu, C.C., Douglas, W.H., DeLong, R., Seong, W.J., Hodges, J., An,
K.N., 2003. Elasticity of alveolar bone near dental implant–bone interfaces after
one month's healing. Journal of Biomechanics 36, 1209–1214.
Checa, S., Prendergast, P.J., 2009. A mechanobiological model for tissue differentia-
tion that includes angiogenesis: a lattice-based modeling approach. Annals of
Biomedical Engineering 37, 129–145.
Coelho, P.G., Granato, R., Marin, C., Bonfante, E.A., Freire, J.N., Janal, M.N., Gil, J.N.,
Suzuki, M., 2010. Biomechanical evaluation of endosseous implants at early
implantation times: a study in dogs. Journal of Oral and Maxillofacial Surgery
68, 1667–1675.
Derhami, K., Wolfaardt, J.F., Faulkner, G., Grace, M., 1995. Assessment of the
periotest device in baseline mobility measurements of craniofacial implants.
International Journal of Oral and Maxillofacial Implants 10, 221–229.
Dong, X.N., Guo, X.E., 2006. Prediction of cortical bone elastic constants by a two-
level micromechanical model using a generalized self-consistent method.
Journal of Biomechanical Engineering 128, 309–316.
Duyck, J., Slaets, E., Sasaguri, K., Vandamme, K., Naert, I., 2007. Effect of intermittent
loading and surface roughness on peri-implant bone formation in a bone
chamber model. Journal of Clinical Periodontology 34, 998–1006.
Duyck, J., Vandamme, K., Geris, L., Van Oosterwyck, H., De Cooman, M., Vanderslo-
ten, J., Puers, R., Naert, I., 2006. The influence of micro-motion on the tissue
differentiation around immediately loaded cylindrical turned titanium
implants. Archives of Oral Biology 51, 1–9.
Folgado, J., Fernandes, P.R., Jacobs, C.R., Pellegrini, V.D., 2009. Influence of femoral
stem geometry, material and extent of porous coating on bone ingrowth and
atrophy in cementless total hip arthroplasty: an iterative finite element model.
Computer Methods in Biomechanics and Biomedical Engineering 12, 135–145.
Franchi, M., Bacchelli, B., Giavaresi, G., De Pasquale, V., Martini, D., Fini, M., Giardino, R.,
Ruggeri, A., 2007. Influence of different implant surfaces on peri-implant osteo-
genesis: histomorphometric analysis in sheep. Journal of Periodontology 78,
879–888.
Friberg, B., Sennerby, L., Grondahl, K., Bergstrom, C., Back, T., Lekholm, U., 1999. On
cutting torque measurements during implant placement: a 3-year clinical
prospective study. Clinical Implant Dentistry and Related Research 1, 75–83.
Geckili, O., Bilhan, H., Cilingir, A., Mumcu, E., Bural, C., 2012. A comparative in vitro
evaluation of two different magnetic devices detecting the stability of osseo-
integrated implants. Journal of Periodontal Research 47, 508–513.
Geris, L., Andreykiv, A., Van Oosterwyck, H., Sloten, J.V., van Keulen, F., Duyck, J.,
Naert, I., 2004. Numerical simulation of tissue differentiation around loaded
titanium implants in a bone chamber. Journal of Biomechanics 37, 763–769.
Ghorayeb, S.R., Bertoncini, C.A., Hinders, M.K., 2008. Ultrasonography in dentistry.
IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control 55,
1256–1266.
Gill, A., Shellock, F.G., 2012. Assessment of MRI issues at 3-Tesla for metallic surgical
implants: findings applied to 61 additional skin closure staples and vessel
ligation clips. Journal of cardiovascular magnetic resonance 14, http://dx.doi.
org/10.1186/1532-429X-14-3.
11
Glauser, R., Lundgren, A.K., Gottlow, J., Sennerby, L., Portmann, M., Ruhstaller, P.,
Hammerle, C.H., 2003. Immediate occlusal loading of Branemark TiUnite
implants placed predominantly in soft bone: 1-year results of a prospective
clinical study. Clinical Implant Dentistry and Related Research 5, 47–56.
Glauser, R., Sennerby, L., Meredith, N., Ree, A., Lundgren, A., Gottlow, J., Hammerle,
C.H.F., 2004. Resonance frequency analysis of implants subjected to immediate
or early functional occlusal loading – successful vs. failing implants. Clinical
Oral Implants Research 15, 428–434.
Goto, T., Yoshinari, M., Kobayashi, S., Tanaka, T., 2004. The initial attachment and
subsequent behavior of osteoblastic cells and oral epithelial cells on titanium.
Biomedical Materials and Engineering 14, 537–544.
Haas, R., Bernhart, T., Dortbudak, O., Mailath, G., 1999. Experimental study of the
damping behavior of IMZ implants. Journal of Oral Rehabilitation 26, 19–24.
Haiat, G., Padilla, F., Svrcekova, M., Chevalier, Y., Pahr, D., Peyrin, F., Laugier, P.,
Zysset, P., 2009. Relationship between ultrasonic parameters and apparent
trabecular bone elastic modulus: a numerical approach. Journal of Biomecha-
nics 42, 2033–2039.
Harle, J., Salih, V., Knowles, J.C., Mayia, F., Olsen, I., 2001. Effects of therapeutic
ultrasound on osteoblast gene expression. Journal of Materials Science:
Materials in Medicine 12, 1001–1004.
Hecht, S., Adams, W.H., Narak, J., Thomas, W.B., 2011. Magnetic resonance imaging
susceptibility artifacts due to metallic foreign bodies. Veterinary Radiology and
Ultrasound 52, 409–414.
Heller, A.L., Heller, R.L., 1996. Clinical evaluations of a porous-surfaced endosseous
implant system. Journal of Oral Implantology 22, 240–246.
Hellmich, C., Kober, C., Erdmann, B., 2008. Micromechanics-based conversion of CT
data into anisotropic elasticity tensors, applied to FE simulations of a mandible.
Annals of Biomedical Engineering 36, 108–122.
Herrero-Climent, M., Albertini, M., Rios-Santos, J.V., Lazaro-Calvo, P., Fernandez-
Palacin, A., Bullon, P., 2012. Resonance frequency analysis-reliability in third
generation instruments: Osstell mentor (R). Medicina Oral Patologia Oral y
Cirugia Bucal 17, E801–E806.
Heybeli, N., Yesildag, A., Oyar, O., Gulsoy, U.K., Tekinsoy, M.A., Mumcu, E.F., 2002.
Diagnostic ultrasound treatment increases the bone fracture-healing rate
in an internally fixed rat femoral osteotomy model. Journal of Ultrasound in
Medicine 21, 1357–1363.
Hong, J., Lim, Y.J., Park, S.O., 2012. Quantitative biomechanical analysis of the
influence of the cortical bone and implant length on primary stability. Clinical
Oral Implants Research 23, 1193–1197.
Hsu, J.T., Huang, H.L., Chang, C.H., Tsai, M.T., Hung, W.C., Fuh, L.J., 2013a. Relation-
ship of three-dimensional bone-to-implant contact to primary implant stability
and peri-implant bone strain in immediate loading: microcomputed tomo-
graphic and in vitro analyses. International Journal of Oral and Maxillofacial
Implants 28, 367–374.
Hsu, J.T., Huang, H.L., Tsai, M.T., Wu, A.Y.J., Tu, M.G., Fuh, L.J., 2013b. Effects of the 3D
bone-to-implant contact and bone stiffness on the initial stability of a dental
implant: micro-CT and resonance frequency analyses. International Journal of
Oral and Maxillofacial Surgery 42, 276–280.
Hsu, S.K., Huang, W.T., Liu, B.S., Li, S.M., Chen, H.T., Chang, C.J., 2011. Effects of near-
field ultrasound stimulation on new bone formation and osseointegration of
dental titanium implants in vitro and in vivo. Ultrasound in Medicine and
Biology 37, 403–416.
Huja, S.S., Katona, T.R., Burr, D.B., Garetto, L.P., Roberts, W.E., 1999. Microdamage
adjacent to endosseous implants. Bone 25, 217–222.
Huwiler, M.A., Pjetursson, B.E., Bosshardt, D.D., Salvi, G.E., Lang, N.P., 2007.
Resonance frequency analysis in relation to jawbone characteristics and during
early healing of implant installation. Clinical Oral Implants Research 18,
275–280.
Ilic, S., Hackl, K., Gilbert, R., 2010. Application of the multiscale FEM to the modeling
of cancellous bone. Biomechanics and Modeling in Mechanobiology 9, 87–102.
Isidor, F., 2006. Influence of forces on peri-implant bone. Clinical Oral Implants
Research 17, 8–18.
Izaguirre, J.A., Chaturvedi, R., Huang, C., Cickovski, T., Coffland, J., Thomas, G.,
Forgacs, G., Alber, M., Hentschel, G., Newman, S.A., Glazier, J.A., 2004. Compu-
Cell, a multi-model framework for simulation of morphogenesis. Bioinformatics
20, 1129–1137.
Junker, R., Dimakis, A., Thoneick, M., Jansen, J.A., 2009. Effects of implant surface
coatings and composition on bone integration: a systematic review. Clinical
Oral Implants Research 20, 185–206.
Karoussis, I.K., Bragger, U., Salvi, G.E., Burgin, W., Lang, N.P., 2004. Effect of implant
design on survival and success rates of titanium oral implants: a 10-year
prospective cohort study of the ITI dental implant system. Clinical Oral
Implants Research 15, 8–17.
Kerner, S., Migonney, V., Pavon-Djavid, G., Helary, G., Sedel, L., Anagnostou, F., 2009.
Bone tissue response to titanium implant surfaces modified with carboxylate
and sulfonate groups. Journal of Materials Science: Materials in Medicine 10,
707–715.
Keyak, J.H., Falkinstein, Y., 2003. Comparison of in situ and in vitro CT scan-based
finite element model predictions of proximal femoral fracture load. Medical
Engineering and Physics 25, 781–787.
Knothe Tate, M.L., 2011. Top down and bottom up engineering of bone. Journal of
biomechanics 44, 304–312.
Knothe Tate, M.L., Falls, T.D., McBride, S.H., Atit, R., Knothe, U.R., 2008. Mechanical
modulation of osteochondroprogenitor cell fate. The International Journal of
Biochemistry and Cell Biology 40, 2720–2738.
Laugier, P., Haiat, G., 2011. Bone Quantitative Ultrasound. Sringer, New York.
12 V. Mathieu et al. / Journal of Biomechanics 47 (2014) 3–13
Laz, P.J., Pal, S., Halloran, J.P., Petrella, A.J., Rullkoetter, P.J., 2006. Probabilistic finite
element prediction of knee wear simulator mechanics. Journal of Biomechanics
39, 2303–2310.
Lee, C.K., Karl, M., Kelly, J.R., 2009. Evaluation of test protocol variables for dental
implant fatigue research. Dental Materials 25, 1419–1425.
Lin, C.L., Wang, J.C., Kuo, Y.C., 2006. Numerical simulation on the biomechanical
interactions of tooth/implant-supported system under various occlusal forces
with rigid/non-rigid connections. Journal of biomechanics 39, 453–463.
Lioubavina-Hack, N., Lang, N.P., Karring, T., 2006. Significance of primary stability
for osseointegration of dental implants. Clinical Oral Implants Research 17,
244–250.
Liu, Q., Liu, X., Liu, B., Hu, K., Zhou, X., Ding, Y., 2012. The effect of low-intensity
pulsed ultrasound on the osseointegration of titanium dental implants. British
Journal of Oral and Maxillofacial Surgery 50, 244–250.
Luo, G.M., Sadegh, A.M., Alexander, H., Jaffe, W., Scott, D., Cowin, S.C., 1999. The
effect of surface roughness on the stress adaptation of trabecular architecture
around a cylindrical implant. Journal of Biomechanics 32, 275–284.
Lynch, J.E., Hinders, M.K., 2002. Ultrasonic device for measuring periodontal
attachment levels. The Review of Scientific Instruments 73, 2686–2693.
Markovic, A., Calvo-Guirado, J.L., Lazic, Z., Gomez-Moreno, G., Calasan, D., Guardia, J.,
Colic, S., Aguilar-Salvatierra, A., Gacic, B., Delgado-Ruiz, R., Janjic, B., Misic, T.,
2013. Evaluation of primary stability of self-tapping and non-self-tapping dental
implants. a 12-week clinical study. Clinical Implant Dentistry and Related
Research 15, 341–349.
Mathieu, V., Fukui, K., Matsukawa, M., Kawabe, M., Vayron, R., Soffer, J., Anagnostou, F.,
Haiat, G., 2011a. Micro-Brillouin scattering measurements in mature and newly
formed bone tissue surrounding an implant. Journal of Biomechanical Engineer-
ing 133, 021006.
Mathieu, V., Soffer, J.E., Anagnostou, F., Haïat, G., 2011b. Numerical simulation of
ultrasonic wave propagation for the evaluation of dental implant biomechani-
cal stability. Journal of the Acoustical Society of America 129, 4062–4072.
Mathieu, V., Soffer, J.E., Anagnostou, F., Haïat, G., 2011c. Ultrasonic evaluation of
dental implant biomechanical stability: an in vitro study. Ultrasound in
Medicine and Biology 37, 262–270.
Mathieu, V., Soffer, J.E., Anagnostou, F., Haïat, G., 2012a. Influence of healing time on
the ultrasonic response of the bone–implant interface. Ultrasound in Medicine
and Biology 38, 611–618.
Mathieu, V., Vayron, R., Barthel, E., Dalmas, D., Soffer, J.E., Anagnostou, F., Haïat, G.,
2012b. Mode III cleavage of a coin-shaped titanium implant in bone: effect of
friction and crack propagation. Journal of the Mechanical Behavior of Biome-
dical Materials 8, 194–203.
Maugis, D., 2000. Frictionless Elastic Contact, Contact adhesion and Rupture of
Elastic Solids. Springer p. 236.
Meredith, N., Alleyne, D., Cawley, P., 1996. Quantitative determination of the
stability of the implant–tissue interface using resonance frequency analysis.
Clinical Oral Implants Research 7, 261–267.
Mericskestern, R., Milani, D., Mericske, E., Olah, A., 1995. Periotest(R) measurements
and osseointegration of mandibular iti implants supporting overdentures – a
one-year longitudinal-study. Clinical Oral Implants Research 6, 73–82.
Meunier, A., Katz, J.L., Christel, P., Sedel, L., 1988. A reflection scanning acoustic
microscope for bone and bone-biomaterials interface studies. Journal of
Orthopaedic Research 6, 770–775.
Michiardi, A., Helary, G., Nguyen, P.C., Gamble, L.J., Anagnostou, F., Castner, D.G.,
Migonney, V., 2010. Bioactive polymer grafting onto titanium alloy surfaces.
Acta Biomaterialia 6, 667–675.
Nedir, R., Bischof, M., Briaux, J.M., Beyer, S., Szmukler-Moncler, S., Bernard, J.P.,
2004a. A 7-year life table analysis from a prospective study on ITI implants with
special emphasis on the use of short implants – results from a private practice.
Clinical Oral Implants Research 15, 150–157.
Nedir, R., Bischof, M., Szmukler-Moncler, S., Bernard, J.P., Samson, J., 2004b.
Predicting osseointegration by means of implant primary stability – a
resonance-frequency analysis study with delayed and immediately loaded ITI
SLA implants. Clinical Oral Implants Research 15, 520–528.
Nkenke, E., Hahn, M., Weinzierl, K., Radespiel-Troger, M., Neukam, F.W., Engelke, K.,
2003. Implant stability and histomorphometry: a correlation study in human
cadavers using stepped cylinder implants. Clinical Oral Implants Research 14,
601–609.
Nomura, T., Gold, E., Powers, M.P., Shingaki, S., Saito, C., Katz, J.L., 2006. A clinical
case report: interface analysis of a successful well-functioning transmandibular
implant from a cadaver mandible. Journal of Biomedical Materials Research.
Part B Applied Biomaterials 77, 213–218.
Ogawa, T., Possemiers, T., Zhang, X., Naert, I., Chaudhari, A., Sasaki, K., Duyck, J.,
2011a. Influence of whole-body vibration time on peri-implant bone healing: a
histomorphometrical animal study. Journal of Clinical Periodontology 38,
180–185.
Ogawa, T., Zhang, X., Naert, I., Vermaelen, P., Deroose, C.M., Sasaki, K., Duyck, J.,
2011b. The effect of whole-body vibration on peri-implant bone healing in rats.
Clinical Oral Implants Research 22, 302–307.
Oh, J.S., Kim, S.G., 2012. Clinical study of the relationship between implant stability
measurements using Periotest and Osstell mentor and bone quality assessment.
Oral Surgery, Oral Medicine, Oral Pathology, and Oral Radiology 113, E35–E40.
Orlik, J., Zhurov, A., Middleton, J., 2003. On the secondary stability of coated
cementless hip replacement: parameters that affected interface strength.
Medical Engineering and Physics 25, 825–831.
Orsini, E., Giavaresi, G., Trire, A., Ottani, V., Salgarello, S., 2012. Dental implant
thread pitch and its influence on the osseointegration process: an in vivo
comparison study. International Journal of Oral and Maxillofacial Implants 27,
383–392.
Ostman, P.O., Hellman, M., Wendelhag, I., Sennerby, L., 2006. Resonance frequency
analysis measurements of implants at placement surgery. International Journal
of Prosthodontics 19, 77–83.
Palou, M.E., McQuade, M.J., Rossmann, J.A., 1987. The use of ultrasound for the
determination of periodontal bone morphology. Journal of Periodontology 58,
262–265.
Park, K.J., Kwon, J.Y., Kim, S.K., Heo, S.J., Koak, J.Y., Lee, J.H., Lee, S.J., Kim, T.H.,
Kim, M.J., 2012. The relationship between implant stability quotient values and
implant insertion variables: a clinical study. Journal of Oral Rehabilitation 39,
151–159.
Pattijn, V., Jaecques, S.V.N., De Smet, E., Muraru, L., Van Lierde, C., Van der Perre, G.,
Naert, I., Sloten, J.V., 2007. Resonance frequency analysis of implants in the
guinea pig model: Influence of boundary conditions and orientation of the
transducer. Medical Engineering and Physics 29, 182–190.
Perez, M.A., Moreo, P., Garcia-Aznar, J.M., Doblare, M., 2008. Computational
simulation of dental implant osseointegration through resonance frequency
analysis. Journal of Biomechanics 41, 316–325.
Pilliar, R.M., Lee, J.M., Maniatopoulos, C., 1986. Observations on the effect of
movement on bone ingrowth into porous-surfaced implants. Clinical Ortho-
paedics and Related Research, 108–113.
Potter, H.G., Nestor, B.J., Sofka, C.M., Ho, S.T., Peters, L.E., Salvati, E.D.A., 2004.
Magnetic resonance imaging after total hip arthroplasty: evaluation of peri-
prosthetic soft tissue. Journal of Bone and Joint Surgery – American 86A,
1947–1954.
Quaresma, S.E., Cury, P.R., Sendyk, W.R., Sendyk, C., 2008. A finite element analysis
of two different dental implants: stress distribution in the prosthesis, abut-
ment, implant, and supporting bone. Journal of Oral Implantology 34, 1–6.
Rabel, A., Kohler, S.G., Schmidt-Westhausen, A.M., 2007. Clinical study on the
primary stability of two dental implant systems with resonance frequency
analysis. Clinical Oral Investigations 11, 257–265.
Raghavendra, S., Wood, M.C., Taylor, T.D., 2005. Early wound healing around
endosseous implants: a review of the literature. International Journal of Oral
and Maxillofacial Implants 20, 425–431.
Rangert, B., Sennerby, L., Meredith, N., Brunski, J., 1997. Design, maintenance
and biomechanical considerations in implant placement. Dental Update 24,
416–420.
Riviere, J., Renaud, G., Haupert, S., Talmant, M., Laugier, P., Johnson, P.A., 2010.
Nonlinear acoustic resonances to probe a threaded interface. Journal of Applied
Physics 107, 124901.
Riviere, J., Haupert, S., Laugier, P., Johnson, P.A., 2012a. Nonlinear ultrasound:
Potential of the cross-correlation method for osseointegration monitoring.
Journal of the Acoustical Society of America 132, EL202–EL207.
Riviere, J., Haupert, S., Laugier, P., Ulrich, T.J., Le Bas, P.Y., Johnson, P.A., 2012b. Time
reversed elastic nonlinearity diagnostic applied to mock osseointegration
monitoring applying two experimental models. Journal of the Acoustical
Society of America 131, 1922–1927.
Rønold, H.J., Ellingsen, J.E., 2002a. Effect of micro-roughness produced by TiO2
blasting-tensile testing of bone attachment by using coin-shaped implants.
Biomaterials 23, 4211–4219.
Rønold, H.J., Ellingsen, J.E., 2002b. The use of a coin shaped implant for direct in situ
measurement of attachment strength for osseointegrating biomaterial surfaces.
Biomaterials 23, 2201–2209.
Rønold, H.J., Ellingsen, J.E., Lyngstadaas, S.P., 2003a. Tensile force testing of
optimized coin-shaped titanium implant attachment kinetics in the rabbit
tibiae. Journal of Materials Science: Materials in Medicine 14, 843–849.
Rønold, H.J., Lyngstadaas, S.P., Ellingsen, J.E., 2003b. Analysing the optimal value for
titanium implant roughness in bone attachment using a tensile test. Biomater-
ials 24, 4559–4564.
Rønold, H.J., Lyngstadaas, S.P., Ellingsen, J.E., 2003c. A study on the effect of dual
blasting with TiO2 on titanium implant surfaces on functional attachment in
bone. Journal of Biomedical Materials Research. Part A 67, 524–530.
Rungsiyakull, C., Li, Q., Sun, G.Y., Li, W., Swain, M.V., 2010. Surface morphology
optimization for osseointegration of coated implants. Biomaterials 31,
7196–7204.
Salawu, O.S., 1997. Detection of structural damage through changes in frequency: a
review. Engineering Structures 19, 718–723.
Salonen, M.A.M., Raustia, A.M., Kainulainen, V., Oikarinen, K.S., 1997. Factors related
to Periotest values in endosseal implants: a 9-year follow-up. Journal of Clinical
Periodontology 24, 272–277.
Sansalone, V., Kaiser, J., Naili, S., Lemaire, T., 2012. Interstitial fluid flow within bone
canaliculi and electro-chemo-mechanical features of the canalicular milieu: a
multi-parametric sensitivity analysis. Biomechanics and Modeling in Mechan-
obiology 12, 533–553.
Sansalone, V., Naili, S., Bousson, V., Bergot, C., Peyrin, F., Zarka, J., Laredo, J.D., Haiat, G.,
2010. Determination of the heterogeneous anisotropic elastic properties of human
femoral bone: from nanoscopic to organ scale. Journal of Biomechanics 43,
1857–1863.
Scarano, A., Degidi, M., Iezzi, G., Petrone, G., Piattelli, A., 2006. Correlation between
implant stability quotient and bone–implant contact: a retrospective histolo-
gical and histomorphometrical study of seven titanium implants retrieved from
humans. Clinical Implant Dentistry and Related Research 8, 218–222.
Schulte, W., d'Hoedt, B., Lukas, D., Muhlbradt, L., Scholz, F., Bretschi, J., Frey, D.,
Gudat, H., Konig, M., Markl, M., 1983. Periotest – a new measurement process
for periodontal function. Zahnärztliche Mitteilungen 73, 1229–1240.
 V. Mathieu et al. / Journal of Biomechanics 47 (2014) 3–13
Sennerby, L., Persson, L.G., Berglundh, T., Wennerberg, A., Lindhe, J., 2005. Implant
stability during initiation and resolution of experimental periimplantitis: an
experimental study in the dog. Clinical Implant Dentistry and Related Research
7, 136–140.
Seong, W.J., Kim, U.K., Swift, J.Q., Hodges, J.S., Ko, C.C., 2009. Correlations between
physical properties of jawbone and dental implant initial stability. Journal of
Prosthetic Dentistry 101, 306–318.
Shalabi, M.M., Wolke, J.G.C., Cuijpers, V., Jansen, J.A., 2007. Evaluation of bone
response to titanium-coated polymethyl methacrylate resin (PMMA) implants
by X-ray tomography. Journal of Materials Science: Materials in Medicine 18,
2033–2039.
Simon, U., Augat, P., Ignatius, A., Claes, L., 2003. Influence of the stiffness of bone
defect implants on the mechanical conditions at the interface – a finite element
analysis with contact. Journal of Biomechanics 36, 1079–1086.
Singhrao, S.K., Nicholson, K., Crean, S., 2012. Informed choices for challenging
specimens when choosing methacrylate resin systems for histology. Micro-
scopy Research and Technique 75, 576–585.
Skripitz, R., Aspenberg, P., 1998. Tensile bond between bone and titanium: a
reappraisal of osseointegration. Acta Orthopaedica Scandinavica 69, 315–319.
Søballe, K., Hansen, E.S., Jorgensen, H.,B.R., P.H., Bunger, C., 1992. Tissue ingrowth
into titanium and hydroxyapatite-coated implants during stable and unstable
mechanical conditions. Journal of Orthopaedic Research 10, 285–299.
Storani de Almeida, M., Dias Maciel, C., Pereira, J., 2007. Proposal for an ultrasonic
tool to monitor the osseointegration of dental implants. Sensor 7, 1224–1237.
Sutpideler, M., Eckert, S.E., Zobitz, M., An, K.N., 2004. Finite element analysis of
effect of prosthesis height, angle of force application, and implant offset on
supporting bone. International Journal of Oral and Maxillofacial Implants 19,
819–825.
Swan, C.C., Lakes, R.S., Brand, R.A., Stewart, K.J., 2003. Micromechanically based
poroelastic modeling of fluid flow in Haversian bone. Journal of Biomechanical
Engineering 125, 25–37.
Sykaras, N., Iacopino, A.M., Marker, V.A., Triplett, R.G., Woody, R.D., 2000. Implant
materials, designs, and surface topographies: their effect on osseointegration. A
literature review. International Journal of Oral and Maxillofacial Implants 15,
675–690.
Szmukler-Moncler, S., Piattelli, A., Favero, G.A., Dubruille, J.H., 2000. Considerations
preliminary to the application of early and immediate loading protocols in
dental implantology. Clinical Oral Implants Research 11, 12–25.
Taborelli, M., Jobin, M., Francois, P., Vaudaux, P., Tonetti, M., Szmukler-Moncler, S.,
Simpson, J.P., Descouts, P., 1997. Influence of surface treatments developed for
oral implants on the physical and biological properties of titanium. (I) Surface
characterization. Clinical Oral Implants Research 8, 208–216.
Tricio, J., Laohapand, P., van Steenberghe, D., Quirynen, M., Naert, I., 1995.
Mechanical state assessment of the implant–bone continuum: a better under-
standing of the Periotest method. International Journal of Oral and Maxillofacial
Implants 10, 43–49.
Tsai, C.L., Chang, W.H., Liu, T.K., 1992. Preliminary studies of duration and intensity
of ultrasonic treatments on fracture repair. Chineese Journal of Physiology 35,
21–26.
Turkyilmaz, I., 2006. A comparison between insertion torque and resonance
frequency in the assessment of torque capacity and primary stability of
Branemark system implants. Journal of Oral Rehabilitation 33, 754–759.
Turkyilmaz, I., Tumer, C., Ozbek, E.N., Tozum, T.F., 2007. Relations between the bone
density values from computerized tomography, and implant stability para-
meters: a clinical study of 230 regular platform implants. Journal of Clinical
Periodontology 34, 716–722.
Ustun, Y., Erdogan, O., Kurkcu, M., Akova, T., Damlar, I., 2008. Effects of low-
intensity pulsed ultrasound on dental implant osseointegration: a preliminary
report. European Journal of Dentistry 2, 254–262.
Valderrama, P., Oates, T.W., Jones, A.A., Simpson, J., Schoolfield, J.D., Cochran, D.L.,
2007. Evaluation of two different resonance frequency devices to detect
implant stability: a clinical trial. Journal of Periodontology 78, 262–272.
Vanegas-Acosta, J.C., Landinez, P.N., Garzon-Alvarado, D.A., Casale, R.M., 2011. A
finite element method approach for the mechanobiological modeling of the
13
osseointegration of a dental implant. Computer Methods and Programs in
Biomedicine 101, 297–314.
Vansteenberghe, D., Tricio, J., Naert, I., Nys, M., 1995. Damping characteristics of
bone-to-implant interfaces – a clinical-study with the Periotest(R) device.
Clinical Oral Implants Research 6, 31–39.
Vayron, R., Barthel, E., Mathieu, V., Soffer, E., Anagnostou, F., Haiat, G., 2011.
Variation of biomechanical properties of newly formed bone tissue determined
by nanoindentation as a function of healing time. Computer Methods in
Biomechanics and Biomedical Engineering 14, 139–140.
Vayron, R., Barthel, E., Mathieu, V., Soffer, E., Anagnostou, F., Haiat, G., 2012.
Nanoindentation measurements of biomechanical properties in mature and
newly formed bone tissue surrounding an implant. Journal of Biomechanical
Engineering 134, 021007.
Vayron, R., Karasinski, P., Mathieu, V., Michel, A., Loriot, D., Richard, G., Lambert, G.,
Haiat, G., 2013. Variation of the ultrasonic response of a dental implant
embedded in tricalcium silicate-based cement under cyclic loading. Journal of
Biomechanics 46, 1162–1168.
Vayron, R., Mathieu, V., Michel, A., Loriot, D., Haïat, G., 2013. In vitro dental implant
primary stability assessment using an ultrasonic method. Ultrasound in
medicine and biology (submitted for publication).
Vesentini, S., Fitie, C.F., Montevecchi, F.M., Redaelli, A., 2005. Molecular assessment
of the elastic properties of collagen-like homotrimer sequences. Biomechanics
and Modeling in Mechanobiology 3, 224–234.
Viceconti, M., Brusi, G., Pancanti, A., Cristofolini, L., 2006. Primary stability of an
anatomical cementless hip stem: a statistical analysis. Journal of Biomechanics
39, 1169–1179.
Viceconti, M., Muccini, R., Bernakiewicz, M., Baleani, M., Cristofolini, L., 2000. Large-
sliding contact elements accurately predict levels of bone–implant micromo-
tion relevant to osseointegration. Journal of Biomechanics 33, 1611–1618.
Wang, S.J., Lewallen, D.G., Bolander, M.E., Chao, E.Y., Ilstrup, D.M., Greenleaf, J.F.,
1994. Low intensity ultrasound treatment increases strength in a rat femoral
fracture model. Journal of Orthopaedic Research 12, 40–47.
Wenz, H.J., Bartsch, J., Wolfart, S., Kern, M., 2008. Osseointegration and clinical
success of zirconia dental implants: a systematic review. International Journal
of. Prosthodontics 21, 27–36.
Winter, W., Heckmann, S.M., Weber, H.P., 2004. A time-dependent healing function
for immediate loaded implants. Journal of Biomechanics 37, 1861–1867.
Wolff, J., 1892. The Law of Bone Remodeling. Springer, Berlin.
Wu, S.W., Lee, C.C., Fu, P.Y., Lin, S.C., 2012. The effects of flute shape and thread
profile on the insertion torque and primary stability of dental implants. Medical
Engineering and Physics 34, 797–805.
Yang, K.H., Parvizi, J., Wang, S.J., Lewallen, D.G., Kinnick, R.R., Greenleaf, J.F.,
Bolander, M.E., 1996. Exposure to low-intensity ultrasound increases aggrecan
gene expression in a rat femur fracture model. Journal of Orthopaedic Research
14, 802–809.
Yosibash, Z., Trabelsi, N., Milgrom, C., 2007. Reliable simulations of the human
proximal femur by high-order finite element analysis validated by experimen-
tal observations. Journal of Biomechanics 40, 3688–3699.
Younesi, M., Bahrololoom, M.E., Fooladfar, H., 2010. Development of wear resistant
NFSS-HA novel biocomposites and study of their tribological properties for
orthopaedic applications. Journal of the Mechanical Behavior of Biomedical
Materials 3, 178–188.
Zhang, X., Torcasio, A., Vandamme, K., Ogawa, T., van Lenthe, G.H., Naert, I., Duyck, J.,
2012a. Enhancement of implant osseointegration by high-frequency low-magni-
tude loading. PLoS One 7, e40488.
Zhang, X., Vandamme, K., Torcasio, A., Ogawa, T., van Lenthe, G.H., Naert, I., Duyck, J.,
2012b. In vivo assessment of the effect of controlled high- and low-frequency
mechanical loading on peri-implant bone healing. Journal of the Royal Society,
Interface 9, 1697–1704.
Zysset, P.K., Guo, X.E., Hoffler, C.E., Moore, K.E., Goldstein, S.A., 1999. Elastic
modulus and hardness of cortical and trabecular bone lamellae measured by
nanoindentation in the human femur. Journal of Biomechanics 32, 1005–1012.