BLOMECHANICAL AND FUNCTIONAL
BEHAVIOR OF IMPLANTS
CLARK M. STANFORD
Dows Institute for Dental Research
College of Dentistry
University of Iowa
Iowa City, Iowa 52242, USA
Adv Dent Res 13:88-92, June, 1999
AbstractThe ability to achieve a long-term stable implant
interface is not a significant clinical issue when sufficient uni- or
bi-cortical stabilization is available. Clinical outcomes studies
suggest that the higher-risk implants are those placed in
compromised cortical bone (thin, porous, etc.) in anatomic sites
with minimal existing trabecular bone (characterized as type IV
bone). In establishing and maintaining an implant interface in
such an environment, one needs to consider the impact of
masticatory forces. These forces, in turn, have the potential to
create localized changes in interfacial stiffness through the
viscoelastic properties of bone. Changes in these properties will
alter the communication between osteocytes and osteoblasts,
leading to an increase in new bone growth, a maintenance of
established bone, or a loss (potentially catastrophic) of either
cortical or trabecular bone. Therefore, a key to understanding
the biomechanical and functional behavior at an implant
interface is to control the extent of anticipated modeling and
remodeling behavior through an optimal implant design
combined with a thorough understanding of how tissues respond
to the mechanically active environment.
Key words: Interface, mechanotransduction, surface
topography, adaptive remodeling.
Presented at the 15th International Conference on Oral
Biology (ICOB), "Oral Biology and Dental Implants ", held in
Baveno, Italy, June 28-July 1, 1998, sponsored by the
International Association for Dental Research and supported
by Unilever Dental Research
S
ince the groundbreaking work of Branemark and his
colleagues (Albrektsson et aL, 1986), the routine use of
endosseous dental implants for the support of dental
crowns, bridges, and dentures has revolutionized the
field of prosthodontic care. With a greater appreciation for
surgical handling of tissues, careful treatment planning, and
restorative options, the use of implants has been assumed to
play a routine role in the modern dentist's armamentarium
(Roos et aL, 1997), without a clear basis for how osseous
tissues respond to biomechanical forces in a process referred to
as "mechanotransduction". Albrektsson et aL, (1986) defined
the successful integration of an implant as being characterized
by: a lack of clinical signs and symptoms of pathology, a lack
of mobility, and a radiographically stable interface.
How can an implant interface be maintained? Long-term
implant interfaces can be maintained only through dynamic
modeling and remodeling processes. ["Modeling" refers to any
net change in bone shape, whereas "remodeling" refers to the
continuous turnover of bone without a net change in shape or
size.] In turn, these processes (adaptive capacity) allow bone to
withstand the errors inherent in clinical procedures while
creating a biological interface capable of supporting clinical
loads over long periods of time. High implant survival rates are
observed for various anatomic regions of the oral cavity,
provided that immediate stability can be ensured through contact
with cortical bone (Bryant, 1998). In the posterior maxilla, in
contrast, there is often a very thin cortex and sparse cancellous
bone characterized by Lekholm and Zarb (1985) as "type IV
bone". Due to the poor structural and architectural properties of
this clinical description of bone, dental implants tend to have a
lower survival rate in the posterior maxilla {e.g., 65-85%) (Jaffin
and Berman, 1991; Lill et aL, 1993; Jemt and Lekholm, 1995;
Blomqvist et aL, 1996; Lindh et aL, 1998). In a recent meta-
analysis of the literature dealing with partially edentulous
implant patients, Lindh et aL, (1998) observed that implant
"success" in the posterior maxilla was less than that in other
regions of the mouth but depended significantly on case
selection. In general, the responses of trabecular bone to the
mechanical environment are a critical factor, especially in the
edentulous posterior maxilla, where the cortical thickness and/or
local material properties of whatever trabecular bone is present
are potentially insufficient to withstand occlusal forces.
To what parameters of mechanical stimuli do bone-formative
cells (osteoblasts) actually respond? An important, if not
practical, purpose of evaluating bony responses to functional
loading is the translation of static occlusal concepts {e.g., long-
axis loading, minimized lateral stresses, etc.) into a language of
mechanical dynamics describing functional adaptive remodeling
(elevated turnover due to stress magnitudes, frequency, duty
cycle, etc.). ["Stress" is used as a general term not intended to
imply engineering stress. Most authors in fact presume that
strain (or deformation) rather than stress stimulates cell and
VOL. IS BlOMECHANICAL BEHAVIOR OF IMPLANTS
tissue adaptation.] It is also important to differentiate occlusal
concepts designed for prosthetic reasons (screw breakage, wear,
etc.) from the impact of occlusion on the dynamic biological
response(s) at the implant interface. This assumption is
commonly made but rarely questioned.
Conceptually, the remodeling ideas of Wolff are often used
to describe the responses of bone to mechanical loads. In the
last century, Von Meyer, Roux, and Wolff were among the
early investigators to recognize the relationship between tissue
loading and adaptation (Roux, 1881; Wolff, 1986; Brand and
Claes, 1989). Von Meyer (1867) observed that the repeating
patterns in bone architecture and trabecular patterns were
aligned along principal compressive and trabecular stress lines.
In turn, these authors suggested that the re-orientation of
trabecula would be governed by principal stress lines such that
a change in the stress patterns would bring about a change in
the bone's architecture (Brand and Claes, 1989). A necessary
feature of this notion is that the trabeculae would cross at right
angles (an observation with many exceptions). Wolff noted that
while trabeculae no longer crossed at right angles to bone
deformities (e.g., disease or fracture), following a period of
time, they generally remodeled to a state where they did. In his
hypothesis, Wolff suggested that trabecular architecture was
dynamic and followed formal if not mathematical rules. It is
important to note that Wolff never actually proposed any actual
formulations, but his conceptualizations are the basis for
modern attempts at explaining remodeling behavior through
iterative finite elemental modeling. Wolffs legacy and its
impact on implant research was the concept of dynamic
adaptive behavior of cortical and especially trabecular bone. It
is through these ideas that the importance of both the local
material properties of bone and the architecture or manner in
which the trabeculae are connected (connectivity) is
established.
Occlusal loading of the natural dentition has an inherent
feedback loop with the PDL proprioceptive fibers to protect the
radicular dentin, cementum, PDL, and alveolar bone from undue
trauma during mastication. This is not the case with the dental
implant interface. In fact, studies by Carr and Laney (1987)
demonstrated that fully edentulous patients are able to deliver
five-fold greater loads to their implant-borne prosthesis, in
comparison with edentulous subjects with complete dentures.
This has been suggested to be due to the patient's inability to
maintain fine distinction (shape, contours, etc.) and
differentiation of occlusal loading during mastication.
Interestingly, even though there is no PDL-like proprioceptive
mechanism with dental implants, Branemark (1997) referred to a
relative change in sensation and neural capacity that was
observed with patients. This adaptation was referred to as
"osseoperception". Osseoperception suggests that a
compensation is possible through an enhancement of periosteal
conduction of spatial and positional information following
loading (stress-mediated changes in cortical shape conveyed to
neuronal cell membranes as a strain [deformation]). In the
periosteum, mechanoreceptors of the Golgi-Mazzoni type are
sensitive to vibration frequencies (from 100 to 300 Hz) which
can be stimulated by cortical bone strains distributed across the
cortical bone's surface upon loading and consequent
89
deformation of the mandible or maxilla. In turn, the capacity of
the periosteum to act as a biological "strain gauge" in effect can
provide the patient with the ability to develop a spatial and
object shape acuity previously thought impossible. This would
occur as the dental implant delivers loads which lead to
consequent periosteal proprioceptive feedback, eliciting, in turn,
a CNS strain-dependent learned response (Rydevik, 1997).
These issues are the basis for implant-mediated osseoperception,
an important means by which a patient's perception of a metallic
implant as "self lead to acceptance of the load-mediated
neuronal stimuli contributed through cortical and cancellous
bone deformation during occlusal loading.
If tissues respond to mechanical loads, the initial issue is to
assess the mechanotransduction/signal transduction pathways
used by osteoblasts and osteocytes. In other words, "What do
cells see?" When one considers the mechanical environment,
there are several ways by which the stimuli can be mechanically
described, including the magnitudes, direction, frequency, duty
cycle, etc., of the strain stimulus. Since bone is a composite
viscoelastic material, the high rates of loading observed during
mastication may increase the effective functional stiffness (E) of
the implant interface. This increase in interfacial stiffness occurs
through a change in local material properties (e.g., increasing
bone mass) as well as through changes in the orientation and
connectivity of trabecular struts in cancellous bone (Mullender
and Huiskes, 1997). The change in stiffness has a number of
implications regarding how tissues perceive the load at the
interface and the degree of functional response. Osteocytes in
cortical and trabecular bone play a role as mechanotransducers
of mechanical forces (Klein-Nulend et al., 1995; Mullender and
Huiskes, 1997; Owan et al., 1997). This occurs through the
detection of local fluid flow within the bone (referred to as
"streaming potentials"), and/or through direct connections to
other cells (especially the cambium layer of the periosteum) and
the extracellular matrix (Mullender and Huiskes, 1997; Owan et
al., 1997). In fact, osteocytes are highly sensitive to fluid shear
forces and as such may play a key sensory role as electrolytic
tissue fluids pass through the canaliculi upon the external
application of tissue stresses (Weinbaum et al., 1994). The
momentary increase in interfacial stiffness, in turn, acts to alter
the degree of mechanical signals perceived by the osteocytes in
the adjacent 1 mm of peri-implant bone. Recent evidence by
Nicolella et al. (1998) suggests that the architectural shape of the
localized matrix around vascular channels (e.g., Haversian
canals) creates larger strain values (up to 3.0%) than those
conventionally measured on the cortical surface (0.013%). Thus,
the physical properties of the matrix can act as part of the signal
relay mechanism in addition to direct cellular communication
with and/or by cytokines.
How do the material properties of bone on implant surfaces
influence biological responses to loading? The osseous
interface of a dental implant responds with a viscoelastic
response to loading. In turn, this surface behavior is imparted
through the control of interfacial shear strains through the
combination of macroscopic and microscopic architecture (e.g.,
roughness) of the titanium oxide interface. The capacity of bone
to respond to the impact forces derived from occlusion
(described by Stanford and Brand [1999] as having high load
90
magnitudes with a high frequency but short duration) suggests
that the local interfacial physical properties will change (in a
viscoelastic manner) such that the interface has the capacity to
increase its local external modulus of stiffness during load
transfer through the osseous interface. This capacity for local
changes in stiffness has two implications: First, the increase in
stiffness (or the principle that it is attempted) could underlie the
observations of Garetto et al. (1995). In their work with
retrieval material, they suggest that the interface never achieves
final establishment of interfacial mechanical properties through
an elevated remodeling response. In part, this was suggested to
be through the repeated activation of Activation-Resorption-
Formation (ARF) phenomena, leading to a lack of complete
secondary mineralization of the extracellular matrix. This
implies that the biological interfaces on alloplastic materials
may adjust local physical properties (load conduction) through
an ongoing alteration of material properties (e.g., mineral
content and the resulting matrix stiffness). Second, the capacity
of the interface to adjust viscoelastically implies a role for strain
rate in biological responses. Recently, Mosley and Lanyon
(1998) and Turner et al. (1995), using in vivo models,
demonstrated that the rate of load application (e.g., a gradual vs.
a rapid rise to peak load magnitude) has a dramatic effect on
trabecular and periosteal proliferation. Lanyon observed that a
rapid rise (0.1 sec to reach 4000 (ji-strain), similar to an impact
load, increased net bone growth by 67% relative to a slower rise
(0.018 sec to 4000 |jL-strain) to the same peak load magnitude.
These studies imply that the biological response to occlusal
loads delivered to the interface are potentially influenced by not
just the loads themselves (peak load magnitudes) but also by
the manner in which the loads are delivered to the osseous
interface. This latter idea implies that tissues are capable of
selectively responding to the masticatory load in such as way as
to adapt and maintain structural integrity, within limits, to the
range of normal daily stimuli. This "small subset" model,
referred to as "temporal processing" by Brand and Stanford
(1994), may be one approach to understanding how cancellous
bone is capable of adapting to the masticatory loads around the
interface.
Load transduction will vary depending on the anatomic
structure of the implant interface. Interfaces that have
essentially a trabecular contact (e.g., type III and especially type
IV situations) will have differences in the ability to maintain a
long-term interface. The lack of cortical bone stabilization may
lead to both elevated micromotion (potentially leading to
fibrous tissue vs. bone) and elevated shear forces at the
interface. One role for surface roughness is to diminish the
effects of shear strains on altering bone remodeling along the
interface. In using an avian ulna model for evaluating cortical
and cancellous remodeling, Qin et al. (1996) observed that
strains consisting of primarily a shear component were
sufficient to maintain remodeling behavior (lack of intracortical
lysis) but would inhibit bone adaptation to the side of an
implant. Buser et al. (1991), Wong et al. (1995), and
Wennerberg et al. (1995, 1996, 1997) observed that
biomechanical measurements of the interfacial strength of an
implant following healing are dependent on surface roughness.
For instance, Wong et al. (1995) observed that pull-out
STANFORD ADV DENT RES JUNE 1999
strengths were highly correlated with two-dimensional
measurements (R a ) of surface roughness (r 2 = 0.90).
Interestingly, the same authors observed only a modest
correlation of "% bone contact" with surface roughness (r2 =
0.56). This suggests that histomorphometric (as well as
radiographic) measurements alone are not a highly predictive
surrogate measurement for biomechanical stability of an
implant interface.
Microscopic surface roughness alone will not control shear
strains at an interfacial surface. The five- to ten-year clinical
outcomes with the TPS-coated cylindrical implant designs
(Haas et al, 1994; Spiekermann et al, 1995; Block et al, 1996)
provide evidence that surface roughness must be optimized and
that the implant design must incorporate architectural design
features to control interfacial shear strains. Control of interfacial
shear strains can be performed by combining macroscopic
levels of implant design (e.g., screw-thread profiles) with
microscopic levels of surface topography (e.g., surface pitting).
To this end, Hansson (1997) biomechanically defined an
optimal surface topography by creating a repeating pattern of 5-
|mm-diameter "pits" on a titanium surface. Each pit had an
average depth of 0.5 jim and a sharp edge profile to allow bone
to grow and establish a microscopically stable osseous "knob".
When this microscopic architecture is combined with a low-
profile macroscopic screw pattern, there was a reduction in
interfacial shear strains. In evaluating this combination,
Gotfredsen et al (1995) used an approach to form these surface
topographies with TiO2 blasting of the bulk cpTi metal and
showed significantly higher removal torque values with the
blasted vs. conventional machined surfaces. In a series of
studies, Wennerberg et al. (1995, 1996, 1997, 1998)
demonstrated that implant surface topography prepared with
TiO2 blasting could create a uniform, reproducible surface
roughness which significantly increased removal torque.
Why would a combination of optimal surface topography
and macroscopic architecture be important? First, in certain
anatomic areas, such as the posterior maxilla, cortical bone is
often very thin (from 400 to 600 fim). Second, following the
placement of an endosseous implant, there will be initial
modeling/remodeling for healing and the establishment of a
biological seal around the neck of the implant. This seal, or
biological "length", is a combination of a 1-1.5-mm junctional
epithelium and a 1.5-2-mm connective tissue region that is
established superior to the alveolar crest (Koka, 1998). Given
that cortical bone will resorb (model) to establish this
biological length, and that this modeling behavior typically
occurs to the level where the screw threads start and/or surface
topography is roughened (Buser et al, 1991; Cochran et al,
1998), an implant designed for use in type IV situations (e.g.,
posterior maxilla) should maintain the maximal amount of
cortical bone (for primary stability) which, in turn, would
allow for the establishment and maintenance of a supporting
trabecular interface.
The achievement of a long-term stable implant interface is
not a significant clinical issue when uni- or bi-cortical
stabilization is available. Clinical outcomes studies suggest that
the higher-risk implants are those placed in compromised
cortical bone (thin, porous, etc.) in anatomic sites with minimal
VOL.13 BIOMECHANICAL BEHAVIOR OF IMPIANTS
existing trabecular bone (characterized by Lekholm and Zarb as
type IV). In establishing and maintaining an implant interface
in such an environment, one needs to consider the impact of
masticatory forces. These forces, in turn, have the potential to
create localized changes in interfacial stiffness through the
viscoelastic properties of bone. Changes in these properties will
alter the communication between osteocytes and osteoblasts,
leading to an increase in new bone growth, a maintenance of
established bone, or a loss (potentially catastrophic) of either
cortical or trabecular bone. Therefore, a key to understanding
the biomechanical and functional behavior at an implant
interface is to control the extent of anticipated modeling and
remodeling behavior through an optimal implant design
combined with a thorough understanding of how tissues
respond to the mechanically active environment.
ACKNOWLEDGMENTS
This investigation was supported in part by USPHS Research
Grant AG15197-01 from the National Institute on Aging,
National Institutes of Health, Bethesda, MD 20892, and by the
Roy J. Carver Charitable Trust, Muscatine, Iowa 52761.
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