DOI: 10.1111/prd.

12291

REVIEW ARTICLE

Effects of occlusal forces on the peri‐implant‐bone interface

stability

Rafael Arcesio Delgado‐Ruiz1 | Jose Luis Calvo‐Guirado2 | Georgios E. Romanos3,4

1
Department of Prosthodontics and Digital Technology, School of Dental Medicine, Stony Brook University, Stony Brook, New York, USA
2
International Dentistry Research Cathedra, Faculty of Medicine and Dentistry, Universidad Catolica San Antonio De Murcia (UCAM), Murcia, Spain
3
Department of Periodontology, School of Dental Medicine, Stony Brook University, Stony Brook, New York, USA
4
Department of Oral Surgery and Implant Dentistry, Johann Wolfgang Goethe University, Frankfurt, Germany

Correspondence
Rafael Arcesio Delgado‐Ruiz, Department of Prosthodontics and Digital Technology, School of Dental Medicine, Stony Brook University, Stony Brook, NY, USA.
Email: rafael.delgado-ruiz@stonybrookmedicine.edu

Editor: Georgios E. Romanos

retention screw, implant body, implant bone interface, and surround‐

1 |  BAC KG RO U N D
The Glossary of Prosthodontic Terms defines occlusion as the ‘act or
process of closure, being closed or shut off and the static relation‐
ship between the incising or masticating surfaces of the maxillary or
mandibular teeth or tooth analogs’.1 To achieve the dental occlusion,
the skeletal and muscular systems work simultaneously to produce
the mandibular movement, which transfers force to the prosthesis,
teeth, implants, and adjacent supporting bone. 2
But the dental/implant occlusion is not just a simple contact be‐
tween opposite surfaces. It is complex, and also includes the friction
of multiple inclined planes and different force vectors (axial and no‐
naxial).3 These force vectors occur simultaneously and are transient
and therefore the concept of a unidirectional occlusal force should
be replaced by the concept of multidirectional occlusal forces.4
Additional forces of swallowing and sometimes parafunctions are
applied to the system and overloading can appear. 2 Occlusal over‐
load has been defined as the load greater than prostheses, implant
components, or interface that tissues are capable of withstanding
without damage.1
For Laney, overload is occurring if the occlusal load exerted
through function or parafunctions exceeds the resistance of the
prosthesis, implant components, implant, and osseointegrated inter‐
5
face, resulting in structural or biological damage. At the biological
level, overload is produced when the amount of force overextends
the adaptation capabilities of the host site. 6 sorption shock mechanism able to reduce the impact of the occlu‐
All the structures subject to occlusal forces can be exposed to
physiological loading or overloading.6 In the case of physiological
loading, forces <3000 microstrains are dissipated through the oc‐
clusal surfaces, prosthetic structure, implant‐abutment connection,
ing, supporting bone (Figure 1).7 Meanwhile, overload strains >3000
microstrains might affect the weakest part of the system producing
structural and/or biological failures.8
The applied occlusal bite forces are extremely difficult to quan‐
tify because they are not absolute and have great variability, which
is influenced by factors such as duration, distribution, direction, and
magnitude of forces.9 Also, other factors such as the number and
location of teeth and implants, their inclinations within the dental
arch, the kind of restoration, and the bone quality can influence the
resultant forces and therefore their accurate measurement.10,11
In relation to the maximum biting forces produced in patients
with osseointegrated implants, different magnitudes of occlusal
forces have been recorded, with values ranging between 25 and
1000 N.12-23 These studies agree that the forces transmitted by the
anterior teeth are lower than those transmitted by the posterior
teeth, that among the posterior teeth the second molar exerts the
maximum levels of force, and that gender influences the bite force,
with higher biting forces being generated by men compared with
women (Table 1).12-23
No matter what magnitude of biting force is applied, the force
will be redirected within the prosthetic and retentive structures
towards the implant body and from there to the implant‐bone in‐
terface, where different stresses and strains will be generated and
extended to a certain distance away from the implant surface. 24-27
Given that the implant‐bone interface does not possess an ab‐
sal loading, all the forces will be absorbed by the interface.9 These
forces produce a mechanical stimulus that has been recognized as
crucial for the maintenance of the osseointegration, or for its break‐
down. 28 Bone load originates the release of cytokines and hormones

Periodontology 2000. 2019;81:179–193. wileyonlinelibrary.com/journal/prd   © 2019 John Wiley & Sons A/S. |  179
Published by John Wiley & Sons Ltd
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180       DELGADO‐RUIZ et al.
A In addition, there is a need to identify etiological factors for bone
B
E1
C The forces transmitted to the implant‐bone interface in a restored
E2
D
E3
F I G U R E 1   The occlusal forces traveling through the implant
system: (A) at the coronal portion, forces of different magnitudes
and directions are applied to the restoration, which dissipate some
of the forces and transfer the others to the abutment/framework;
(B) the forces travel from the abutment/framework to the retention
screw, implant platform, and internal walls of the implant‐abutment
connection; (C) the retention screw transfers forces to the inner
walls of the implant; (D) depending on the forces’ main vector,
the implant body will receive forces at the coronal or apical
portion, and bending moments can be experienced; then the
forces are transmitted to the implant‐bone interface in the form
of compressive or shear forces at the coronal (E1), middle (E2), and
apical thirds (E3), and finally are distributed within the surrounding
bone
that alter the bone strength through changes in the bone mineral
content, bone mass, and bone remodeling rates. 29
The ideal occlusal forces might produce adaptive bone remod‐
eling characterized by increased bone‐to‐implant contacts and en‐
hanced osseointegration.30,31 Therefore, is essential to review the
effects of the occlusal forces at the bone‐implant interface and the
cellular responses to the mechanical load responsible for the main‐
12
tenance of the osseointegration.
Many studies using different animal models have been used
to explain the effects of loading as well as overloading on the
peri‐implant tissues. The anatomical conditions, the experimental
protocol, the implant design, and the presence or lack of plaque
control may be contributing factors, and thus may modify the ex‐
pected outcomes.
Therefore, the purpose of this review is 2‐fold: to explain com‐
prehensively the current literature concerning occlusal loading and
its transfer to the implant‐bone interface, and to describe the bone
dynamics (mechano‐transduction mechanisms) that maintain the health
of the peri‐implant bone of osseointegrated implants under occlusal
forces.
alterations and how these bone changes can be controlled to im‐
prove clinical success.
2 | LOA D I N G TH E I M PL A NT‐ B O N E
I NTE R FAC E
implant are multidirectional (different amounts of axial, nonaxial,
and transversal loads) with a predominance of axial direction during
closure and a combination of axial, nonaxial, and transversal direc‐
tions during the mastication cycle and excursive movements.3 The
functional mastication loads and the parafunctional loads are concen‐
trated and transferred to the surrounding bone through the implant‐
bone interface.32 When the axial loading is predominant, compressive
stresses are transmitted to the implant apex, thus generating a mini‐
mal component of stresses at the cortical bone. Meanwhile, off‐axial
load and transverse loads produce a combination of compressive
stresses at the side of the applied load and large tensile stresses on
the opposite side of the applied load at the cortical area, and in the
transition between the cortical and cancellous bone.33,34
The compressive and tensile stresses are then redistributed
within the cortical bone and inside the trabecular network, which
is influenced by the bone quality, bone architecture, implant dimen‐
sions, geometry, and material properties.34-36 The magnitude of the
transferred stresses is strongly correlated with the cortical bone
thickness.37 More thickness results in a decrease of the maximum
stress values at the cortical bone.37,38 In addition, the trabecular
bone microstructure can disperse the stress and strain and function
as a load buffer through the trabecular network39 and the basal bone.
Compressive forces of a certain magnitude can increase the
bone density and bone strength over time; meanwhile, shear forces
are associated with higher reabsorption rates.40 A balance between
compressive and tensile forces and minimal shear forces is desirable
for the stability of the bone‐implant interface.40,41 Thus, a perma‐
nent interaction is created between the implant under load and the
surrounding bone, in which the intensity and direction of the ap‐
plied loads dictate the repair and remodeling processes, as well as
the bone destruction.42,43 Recent studies have established that bone
stresses of about 2.0 MPa will result in bone formation; meanwhile,
stresses exceeding 4.0 MPa will result in bone loss.44
The mechanical stimulation perceived by the surrounding bone and
the resultant stresses around loaded implants will be influenced by the
implant design, implant surface, and changes in the bone quality.45 Given
that in vivo acquisition and quantification of the multiple influencing vari‐
ables are extremely difficult to achieve, finite element analysis and a few
animal studies have provided valuable information in this regard.46
Natali et al47 stated that to understand the bone‐implant inter‐
action phenomena then the following information is required: first,
DELGADO‐RUIZ et al. |
      181

TA B L E 1   Maximum bite forces registered at implants in different clinical studies. Values are highly variable because of the multiple
factors that can influence the magnitudes of the forces

Maximum Type of antagonist Gender

bite forces in
patients with IFDP/
implants Global C/IOD IFDP C/C D/D Anterior Premolar Molar Men Women

Carlsson and 42‐412 N                  

Harldsson12
Carr and 112.9 N                  
Laney13
Mericske‐             200 300 N    
Stern and NFirst Second
Zarb14 premo‐ molars
lars and
first
molars
Fontijn‐           25‐170N   50‐400 N    
Tekamp Molar
et al15 region
Raadsheer                 545.7 383.6
et al16 N N
Duyck et al17 776.7 N         The authors reported that the mean of occlusal contacts is
Mean mag‐ 26.1 sites in humans, and the magnitude of each occlusal
nitude of the contact is 26.2 N
occlusal force
Morneburg 91‐129 N                  
and
Pröschel18
Luraschi 125.5 N                  
et al19
Müller et al23   88.1 ±  270 ±  61.4 ±  354.1 ±           
61.20 N 211.6 N 57.8 N 181.4 N
Baca et al20 516.58 ± 85.58                  
N
Sumida 58.8 N                  
et al21
Elsyad and 98.57 N                  
Khairallah22

C/C, complete denture/complete denture; C/IOD, complete denture/implant overdenture; D/D, dentate arch/dentate arch; IFDP/IFDP, implant‐sup‐
ported fixed dental prosthesis; N, Newtons.

an accurate numerical model including the complex geometry of
each dental implant design and, second, the anatomy and bone mi‐
crostructure characteristics of the future implant bed obtained from
improved cone beam computed tomography/computed tomography
data. This information will provide a prediction of the stress and
strain and will enhance the treatment approaches.47
3 | I M PL A NT D E S I G N A N D LOA D
TR A N S FE R
Although different studies have shown that the external loads are
transferred to the surrounding cortical, cancellous bone and api‐
cal area, most of the external load is transferred to the cortical
bone.48,49 Given that the profile of a dental implant influences the
load transfer, thus, by modifying the external contour of an implant,
the load transfer could be reoriented and redistributed.50
The external contour can be improved by increasing the implant
diameter and length because the increment of the implant area re‐
duces the magnitude of the interfacial stresses.50,51 Specifically, the
increment in the implant diameter will reduce the interfacial stresses
at the cortical bone; meanwhile, the increment of the implant
length will reduce the interfacial stress gradients at the cancellous
region.52,53
Different methods have been introduced to control and reduce
the stresses around the implant body. Examples of this are changes
to the implant neck, design changes to the implant thread configura‐
tions, and implant surface modifications.41,49,54-86
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182       DELGADO‐RUIZ et al.

First, there is a stress transferring mechanism, which reduces the

3.1 | Changes to the implant neck design
Given that this is a region of highly concentrated mechanical
stresses, where bone reabsorption usually occurs,54 the modifi‐
cations introduced at the implant neck are focused on the reduc‐
tion of the stresses, such as tensile and shear forces at the cortical
area (Figure 2).55 These modifications are platform switching and
microthreads.
Platform switching configurations exhibited effective stress per‐
formance and reduced the risk of overloading showing less crestal
bone loss of cortical bone compared with nonplatform switching de‐
signs.52 Finite element analysis studies showed that oblique forces
directed to implants with platform switching resulted in a reduction
of maximum von Misses, compressive, and tensile stresses compared
with conventional design. This was explained by a redistribution of
the stresses to the palatal side of the platform, the entire implant
surface, and the shifting of the stresses from the compact bone area
towards the cancellous bone area.56
Maximum stresses at the cortical area were lower in implants
with platform switching compared with conventional implants. The
implants with platform switching showed 36% stress reduction with
57
axial loads and 40% with oblique loads. Also, in another study,
platform switching was compared with regular platform diameter
and wide platform diameter implants, and it was found that platform
switching reduced von Mises, compressive, and tensile stress values
in the peri‐implant bone.58 The stresses’ reduction/change at the
neck of the implants with microthread features has been explained
by 4 different mechanisms.
stresses at the cortical area. Apparently changes in the implant pro‐
file by the incorporation of microthreads can induce changes in the
direction of the interfacial stresses.59
The second mechanism is the capability of the microthreads to
withstand and transform axial and off‐axial loads, which leads to
more compressive stresses and less shear stresses.60 Apparently a
dental implant with a microthreaded neck that receives an axial load
of 100 N can reduce the maximum stress values transferred to the
cortical area by up to 6.25 MPa compared with a conventional im‐
plant without microthreads, which presented maximum stress val‐
ues of 12 MPa.61
The third mechanism is based in the microthread geometry, which
seems to exert a particular influence in the reduction of the maximum
stresses: V‐shaped microthreads produced greater stress dissipation in
finite element analysis and better bone remodeling patterns in rabbit's
femur compared with power thread‐shaped microthreads.62
The fourth mechanism resulting from the presence of micro‐
threads is the increment of the surface area, producing an increment
in the bone‐implant contact,63 which could at the same time influ‐
ence the stress distribution towards a larger surface of peri‐implant
bone, and therefore might reduce the marginal bone loss.64
3.2 | Changes to the implant thread design
The thread design includes the thread pitch, depth, and shape (in‐
cluding the angle of the upper and lower thread flanks) (Figure 3).
Also, different thread geometries are available (eg, trapezoidal,

A B C

D E F

F I G U R E 2   Different neck designs will have a different stress transfer and display different mechanical behavior on the surrounding bone:
(A) microthreaded neck of 1 mm; (B) polished neck of 1.5 mm; (C) expanded neck with larger diameter than the implant body; (D) expanded
polished neck of 2 mm; (E) expanded neck with polished collar of 0.7 mm; (F) microthreaded neck of 2 mm
DELGADO‐RUIZ et al. |
      183

and to favor the dissipation of stresses at the bone‐implant interface

(Figure 4).65,66
Modifications to the implant thread designs can change the stress

D patterns at the surrounding bone, especially at the cancellous area

B showed that the thread shape contributed to the reduction of stress
A found that the square‐shaped threads transformed the shear forces
C
F I G U R E 3   The threads are protrusions that emerge from
the implant walls which anchor, stabilize, and facilitate the force
transference to the surrounding bone: (A) thread pitch, distance
from the tip of 1 thread to the tip of the adjacent 1; (B) thread
geometry, the blue shadowed area indicates a V‐shape thread; (C)
inter‐thread depth, variable depth from a line connecting the tip of
2 adjacent threads to the implant wall; (D) valley, the area between
2 threads
squared, V‐shaped, power thread, double helix, and reverse but‐
tress); the differences in the thread design are intended to maximize
the initial contact (primary stability), to increase the surface area,
of an osseointegrated implant.52,67,68 Recent studies from Calì et al67
peaks in the trabecular bone in both the early and late stages of the
osseointegration; their results showed that rectangular threads with
6° inclination compared with threads with trapezoidal 30° and 45°
inclination reduced stress peaks by up to 62%. In addition, it was
in force vectors with more axial components.52,68
The dimensions of the threads can influence the stress levels:
longer threads (threads with more depth), which have increased
surface/contact area with the bone, produced greater stability and
fewer stresses compared with smaller threads with a shorter pitch
length.69 This fact was corroborated by Trisi et al,70 who found that
large‐thread implant designs improved bone anchorage mechani‐
cally and histologically compared with small‐threaded implants. In
addition, the threads should transform undesirable stresses (shear
and tensile forces) into desirable stresses (compressive forces).41
However, not just the thread length and configuration, but also the
bone condition may have a dominant effect on the implant thread
design for the stress dissipation.71
In general, all of the thread designs transfer forces to the inter‐
face and to the surrounding bone, but the location of the forces dif‐
fers.71 Under dominant static axial forces the remodeling activity is
increased at the inner thread region; however, under dominant no‐
naxial forces, the remodeling activity increases at the tip and lower

F I G U R E 4   Examples of different thread geometries: (A) trapezoidal, rounded tip; (B) square threads; (C) reverse buttress threads; (D) V‐
shaped, narrower tip; (E) plateau threads, larger threads compared to the other threads in the figure
 |
184       DELGADO‐RUIZ et al.
flanks of the threads,72 and therefore the bone remodeling patterns
might differ between different thread designs.71-73
Finally, animal and finite element experiments suggest that the
first thread at the coronal part of the implant adjacent to the cortical
bone bears more stresses than the second and third threads, and that
this, together with other factors, may explain the bone remodeling
49
observed after the implant loading to the level of the first thread.
In relation to the influence of thread dimensions and inter‐thread
distances (pitch) on stress distribution, different finite element
analyses found that the most effective stress distribution was produced
when the width of the thread end and the height of the thread were 0.5
p and 0.46 p, respectively (where p = the screw pitch).49,74 Also, it was
demonstrated that reducing the screw pitch was an effective way to
74
reduce the maximum effective stress at the peri‐implant bone.
3.3 | Changes to the implant surface roughness
The implant shape/macrogeometry/design is responsible for the im‐
plant stability and for the stress distribution at the implant‐bone inter‐
face; but the roughness of the implant surface can also influence the
stress pattern, the bone organization, and the cell interactions at the
surrounding tissues.65 It is well known that the osseointegration phe‐
nomenon occurs at a higher rate on roughened surfaces compared
with machined surfaces. In addition, a rough surface can improve cell
adhesion, attachment, spreading, and protein synthesis.76,77 If the os‐
seointegration improves under certain surface and loading character‐
istics then the biomechanical quality of the bone might be improved,
resulting in harder and stiffer implant‐bone interfaces.78
79
Shalabi et al reviewed the effects of the implant surface rough‐
ness on the bone response, and found that the bone‐implant contacts
were higher in roughened vs. machined surfaces. Furthermore, the
type of surface roughness modifies the stresses at the bone‐implant
interface: von Mises stress data showed better stress distribution with
moderate roughened surfaces compared with machined surfaces,
which might result in decreased peri‐implant bone loss.80 The fatigue
behavior of the bone‐implant interface was analyzed for the most com‐
mon implant surfaces obtained after acid‐etching, spark anodization,
F I G U R E 5   Examples of 4 different
implant surfaces observed with a confocal
laser scanning microscope at 100×: (A)
titanium plasma‐sprayed surface; (B)
grit‐blasted and acid‐etched surface; (C)
oxidized titanium surface; (D) machine‐
turned titanium surface. These surfaces
possess different roughness values, with
surface (A) being the roughest, followed
by (C), (B), and (D)
and sandblasting.81 The results showed that the surface obtained with
the sandblasting technique improved the fatigue life and the mechan‐
ical retention from the bone to the implant surfaces significantly more
compared with the acid etching and spark anodization techniques.81
Different implant surface roughnesses have different capabilities
for the distribution of stresses to the implant‐bone interface.80,82 This
is because these differences in roughness produce different friction
coefficients, and those surfaces with higher friction coefficients are
responsible for the bone‐implant interlocking, therefore favoring
stress dissipation. 83,84 Apparently rougher and porous titanium sur‐
faces acquire elastic properties, closer to those of bone, and facili‐
tate stress shielding at the surrounding bone.85 Meanwhile, smooth
machined surfaces with low friction coefficients transfer more shear
forces to the adjacent bone.84,85 Examples of different implant sur‐
faces with differences in roughness are presented in Figure 5.
Recent research has demonstrated that if the surface roughness
is porous and has a trabecular porous structure then the Young mod‐
ulus will be similar to the native bone, thus reducing the stiffness
mismatch between bone and titanium; this factor might increase the
longevity of titanium implants (see Figure 6 for a typical trabecular
metal porous titanium structure).86
4 | TR A N S M I S S I O N O F FO RC E S TO TH E
B O N E‐ I M PL A NT I NTE R FAC E
The forces transferred to the implant‐bone interface will influence
the bone remodeling through different cellular processes87; these
initial mechanical signals will initiate a sequence of biochemical
reactions, which modulate bone formation and resorption. Static
compressive forces even greater than 120 MPa produce a lower
osteoclast response compared with dynamic forces of lower mag‐
nitudes.88 The appropriate biomechanical safety margin to avoid
the initiation of the osteoclastic response induced by overload was
calculated by Ikumi and Tsutsumi89 and was identified as the allow‐
able stress formula where allowable stress (δa) is equal to the critical
stress (δb) over the biomechanical safety factor (S).
DELGADO‐RUIZ et al. |
      185

F I G U R E 6   Confocal laser scanner

image of a porous trabecular metal
implant obtained with a magnification of
200× within an area of 1.2 ± 0.3 mm2.
Multiscale titanium structures seem to
interact better with the surrounding bone

F I G U R E 7   A simplified scheme of the

bone‐remodeling computational scheme
modified from Berli et al.92 A force is
applied axially to the implant, the forces
are redirected by the implant threads, and
stresses are created at the bone‐implant
interface. The stresses activate the bone‐
forming units which, through mechanisms
of balance of bone resorption and bone
formation, will obtain the equilibrium.
Factors, such as mechanical properties
of the trabecular bone, mineral density,
and overload may indicate a more active
resorptive stage

To explain the bone remodeling processes at a mechanical level,
a computational model was proposed90,91; in brief, a specific volume
of bone (sample) is divided into consecutive volumes (bone matrix and
pores), and external loads activate mechanical signals, which stimulate
the bone‐forming units to form and resorb bone with different alter‐
nates, depending on the bone mineral density of the sample (Figure 7).92
The occlusal forces are sensed by bone, thanks to the mechanism
of mechano‐transduction.93 Apparently the cells respond to the envi‐
ronment, changing their biological and biochemical reactions under
94
loading conditions. You et al stated that deformations of the bone tis‐
sue induce strain, which is perceived and transferred to the bone cells.
If the bone deformations are between 0.15% and 0.3% then bone mass
is increased in vivo. At the cellular level, much larger strains of up to
10% are required to initiate the osteogenic response.95 Thus, cells, as a
result of strains near the osteocyte lacunae and microcracks produced
within the bone microstructure, could stimulate osteoblastic activity.96
Rubin et al97 described the bone as capable of optimizing its struc‐
ture under exogenous load, and therefore bone reactions, such as bone
flow, bone deformation, and bone mineralization could precede the
bone fracture as mechanisms of bone adaptation. These mechanisms
are based on a complex strain‐driven regulatory process of different
bone cells and their matrix components.98,99 According to new theo‐
ries applied to dental implants (the failure envelope concept32), when
the implant is osseointegrated and in function and more bone‐implant
contact is achieved (higher coefficient of friction), then a more effi‐
cient load transfer is reached and the failure envelope is reduced by
the reduction of the stress shielding. However, when the bone to im‐
plant contact is reduced and the lateral load levels are dominant, then
the failure envelope is increased and bone loss will increase.32
Studies of implant loading under different conditions were applied
in experimental studies in monkeys. Romanos et al analyzed the effect
of 3 different loading conditions on the peri‐implant bone. The first
group of implants was submerged, the second group was loaded after
3 months of healing, and the third group was immediately loaded. The
results showed increased bone formation and thicker cortical bone at
the loaded groups (especially the immediate loading group) compared
with the submerged group. The authors concluded that implant load‐
ing promotes bone formation and is a key factor in osseointegration.99
Other studies showed that, histologically, the bone changed its micro‐
structure and increased its density under certain load magnitudes100;
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186       DELGADO‐RUIZ et al.

B E

A
C D

F I G U R E 8   Multiscale porosity distribution within the trabecular and cortical bone spaces: (A) panoramic view of a sagittal resin
embedded bone section of dog jaw at the premolar region. The thickness and porosity can be appreciated macroscopically; (B) close view
of the trabecular bone‐cortical bone interface and the changes at the porous scale; (C) slide obtained from the same bone sample stained
with picrosirius red, the interconnected bone trabeculae are observed together with some degree of initial bone organization; (D) higher
magnification of the osteons, showing concentric cement lines and osteocytes; (E) higher magnification showing 2 osteocyte lacunae and
their spaces and some osteocyte prolongations

apparently compressive strain, tensile strain, hydrostatic pressure,
shear strain, and fluid dynamics are some of the variables modulating
101
the bone regeneration under mechanical load.
Much of the bone regeneration results from osteoblast‐osteo‐
clast interactions, driven by the osteocytes and the fluid mechan‐
102
ics occurring through the bone porosities. The bone porosities
are distributed within the Volkmann and Haversian canals (diam‐
eter ± 20 μm), the system of canaliculi, the osteocytes processes
(diameter ± 0.1 μm), and the spaces between hydroxyapatite crys‐
103
tals (diameter 0.01 μm) (Figure 8).
The loaded implant forms a dynamic complex in which forces, ma‐
terials, interfaces, bone tissue, and cells interact in an orchestrated
manner, to achieve and maintain the osseointegration, the stability of
103
the implant, and proper bone function over time. The cells that par‐
ticipate in this mechano‐transduction phenomenon are osteocytes, os‐
teoblasts, osteoclasts, and undifferentiated stem cells. These groups of
cells present variable reactions to tensile and compressive forces.104-106
107
Allori et al stated that the collective efforts of this group of
cells replace the old microdamaged bone with new and mechanically
much stronger bone in a process of constant repair.
5 |  M EC H A N O ‐TR A N S D U C TI O N
PH E N O M E N A AT TH E PE R I ‐ I M PL A NT‐ B O N E
I NTE R FAC E
The occlusal forces are sensed by the bone, thanks to the mechanism
of mechano‐transduction, which is the process of load transformation
into biological and biochemical reactions.108 This phenomenon is fun‐
damental in the establishment of tissue homeostasis.109 The move‐
ment of the interstitial fluid, which occupates ± 20% of the body
mass, is distributed in the extracellular matrix and bone interstices;
it provides waste removal and stimuli transmission and can enhance
the transport of growth factors, cytokines, and another molecules,
which are essential for the metabolism of cells.110-112 Compared with
the major part of the soft tissue, the bone tissue generates greater
flow rates of interstitial fluid induced by muscle contractions, blood
pressure, and mechanical loading.113,114
Pressure gradients in the interstitial fluid drive and force the
fluid from regions of compression to regions of tension.115 This fluid
movement through the multiscale porosity of the trabecular and cor‐
tical bone creates fluid shear forces that stimulate the osteocytes.
Weinbaum hypothesized that fluid shear‐strain forces on actin fil‐
ament and tethering fibers (fibers which anchor the osteocyte cell
processes to the canalicular walls and center them within the cana‐
liculi) are responsible for the stimulation of the osteocytes.116
Cells involved in mechano‐transduction interactions in bone are
osteoblasts, osteocytes, and osteoclasts.106,117 Also, the mesenchy‐
mal stem cells present in the bone marrow are mechano‐sensitive;
for example, the mechano‐sensitive calcium channel transient re‐
ceptor potential subfamily V member 4 in mesenchymal stem cells is
localized in areas of increased strain, specifically the primary cilium.
When the primary cilium is stimulated through oscillatory fluid shear,
calcium signaling and early osteogenic gene expression are initiated
by the mesenchymal stem cells.118 Thus, the bone cells’ interactions
maintain the bone homeostasis through the remodeling process.
DELGADO‐RUIZ et al. |
      187

C D H

F
A
I J
G

F I G U R E 9   Mechanism of the mechano‐transduction force through the osteocytes network. Bending moments are transmitted to the
bone attached to the implant surface. The bone mineralized matrix is deformed in different degrees and fluid flow is stimulated through the
canalicular system. Different interactions will occur between the cells which will stablish bone remodeling: (A) implant thread; (B) organized
bone; (C) trabecular bone; (D) connective tissue; (E) bone‐implant interface; (F) mineralized matrix; (G) osteocyte and their cytoplasmatic
prolongations within the canaliculi; once stimulated the osteocyte will coordinate other cells; (H) osteoblasts; (I) osteoclasts; (J) osteoblast
and osteoclast precursors. Different cytokines and molecules are involved in the interactions occurring between osteocyte‐osteoblast,
osteocyte‐osteoclast, osteocyte‐osteoblast precursors, and ostocyte and osteoclast precursors, oncostatin, regulation of bone formation
and resorption, wingless/integrase gene that participates in cell proliferation, differenciation, migration and ageing also is involved in tissue
homeostasis and inflammation

The bone cells (osteoblasts, osteocytes, and osteoclasts) partic‐
ipate in the remodeling process in different parts of the skeleton
asynchronously, guided by locally generated and regulated general
factors to ensure appropriate communication mechanisms among
the participating cells.119 The balance between new bone tissue
synthesis (osteoblasts), dissolution of the bone matrix (osteoclasts),
and the osteocytes orchestrating the activity of osteoblasts and os‐
teoclasts is as a response to mechanical loading and other factors
(Figure 9).120-122
It is accepted that the strain is applied directly to cell attachments
and that the fluid flow is perceived by the cell membrane.104 The
123
cells react to both mechanisms (fluid flow and mechanical strain),
but responses to fluid flow are greater than responses to mechani‐
cal strength.94 Freund et al124 compiled the factors that have been
related to the mechano‐transduction system in a bone cell. These
factors are fluid flow, matrix strain, connexins, ion channels, primary
cilium, glycocalyx, cell cytoskeleton, and integrins.124 The cell re‐
sponses are induced by the interaction of these factors (Figure 10).
The interaction between extracellular matrix, membrane integ‐
rins, and cell cytoskeleton is fundamental for mechano‐transduction
in bone. Integrins are glycoproteins bonded to the cell membrane
that allow transmission of physical stimuli from the extracellular ma‐
trix to the membrane.125 Afterwards, the cell membrane transfers
deformation to the cytoskeleton. The cytoskeleton is composed of

F I G U R E 1 0   Factors involved
in cell mechano‐transduction: (A)
multidirectional forces; (B) fluid flow;
(C) ion channels; (D) primary cilium; (E)
connexins; (F) cytoeskeleton; (G) integrins
 |
188       DELGADO‐RUIZ et al.
actin, microtubules, and intermediate filaments, and connects the
components of the mechano‐sensing system. The cytoskeleton then
stimulates the nucleus, which starts changes in gene expression.
Other mechano‐sensors are the primary cilium (microtubule ex‐
tension emerging from the cell membrane of bone cells), which sense
changes in the flow of the interstitial fluid127; the glycocalyx (cellular
coating composed mainly of hyaluronic acid), which contributes to
mechano‐transduction, transferring forces to the cytoskeleton and
128,129
integrins ; the connexins (other membrane‐bound proteins,
which connect adjacent cells), which allow exchange of molecules
and participate in osteocyte communication94; and finally the mem‐
brane channels, which are sensitive to fluid flow and membrane
stretch, and respond to mechanical stimulation by allowing exchange
of ions.130
6 |  E FFEC T S O F M EC H A N I C A L LOA D O N
B O N E C E LL S
6.1 | Osteoblasts
Osteoblasts are bone‐forming cells derived from mesenchymal
131,132
stem cells. Their differentiation is driven by mechanical and
biochemical factors and is controlled by the Wingless integrase
gene pathway, which can be activated by hormones and mechani‐
106,133
cal load. The preosteoblast morphology resembles a fibro‐
blast and does not synthesize bone matrix; meanwhile, the shape of
134
a mature osteoblast is cubical and synthesizes bone matrix.
osteoblast controls the synthesis of bone matrix and its mineraliza‐
tion, and also acts through paracrine effects on the bone resorption
induced by the osteoclast.135 Their lifespan goes up to 100 days,136
and after that period the osteoblast can follow 3 pathways: (a) os‐
teocyte differentiation; (b) inactivation and transformation into a
bone‐lining cell; and (c) apoptosis.137
Osteoblasts under high shear stress (0.5 and 2 Pa) can experi‐
ence biochemical changes as, for example, the increment in intra‐
cellular calcium, inositol triphosphate, nitric oxide, prostaglandin
E2, and adenosine triphosphate.138-140 In addition, increased fluid
flow can induce the osteoblasts to express genes for osteopontin,
141-143
cyclooxygenase‐2, and collagen type I. Under low fluid flow,
the osteoblasts have higher proliferation and increased expression
144-146
of genes for Runx2, alkaline phosphatase, and osteocalcin.
6.2 | Osteocytes
The osteocyte is a differentiated osteoblast trapped within the bone
134
matrix. During its differentiation, the osteoblast's body dimen‐
sions are reduced and cytoplasm prolongations are irradiated to the
unmineralized matrix.147 After the mineralization of the matrix, the
gene expression of alkaline phosphatase, type I collagen, and bone
morphogenetic protein‐2 are reduced; meanwhile, the synthesis of
proteins such as osteocalcin, sclerostin, and dentin matrix protein‐1
are increased.148 Of the bone cells, the osteocytes are the most
common and abundant cells (90%‐95% of the total) and respond to
mechanical loading by regulating the activity of the osteoblasts and
osteoclasts.111,114
126
The osteocyte after loading releases soluble factors that control
bone remodeling.120 Among the factors released by the osteocytes
are Ca2+, adenosine triphosphate, nitric oxide, and prostaglandin
E2.149-151 Furthermore, the osteocyte regulates the RANKL, osteo‐
protegerin, and the expression of sclerostin as a result of the fluid
flow within the peri‐canalicular system.152,153 The networks formed
by the cytoplasmatic processes of the osteocytes under loading are
elongated and connect the osteocytes with all the bone cells (with
other osteocytes, with osteoblasts, and with the cells at the bone
surface).154 The communication between osteocytes and the other
cells occurs through gap junction channels (connexins);154 also, the
osteocyte can regulate osteoblast proliferation and differentiation,
and can induce alkaline phosphatase expression in the osteoblast
under mechanical loading.155,156
6.3 | Osteoclasts
Osteoclasts are multinucleated cells derived from mononuclear cells
located in the bone marrow, and are located on endosteal surfaces, in
the Haversian system, and beneath the periosteum. 157 They are spe‐
cialized cells, and their secretions (acids and enzymes) can dissolve
mineralized matrix.158 Cytokines produced by osteoblasts (RANKL
and macrophage colony‐stimulator factor) control their differentia‐
tion and can be inhibited by the secretion of osteoprotegerin.159
The Lack of mechanical stimuli and traumatic loading can both re‐
sult in osteoclast‐induced bone resorption, but the mechanism is still
not well understood.160,161 Apparently, the osteoclast's appearance
depends on the intensity of the bone strain (bone deformation) in
a given area within the bone tissue.162 Studies in mice showed an
increased number of osteoclasts and higher resorption rates in con‐
tinuous overloaded palatal bone. Therefore, the authors concluded
that the osteoclastic resorption is location‐dependent and is sensi‐
tive to the local strain intensity.163
Other factors that can influence the osteoclastogenesis and os‐
teoclast activity are the presence of apoptotic osteocytes and me‐
chanical signals expressed by active osteocytes,164 and the presence
of sclerostin on the compression site, which promotes the osteoclast
activity by increasing RANKL expression at osteocytes.165
7 | CO N C LU D I N G R E M A R K S
This review aimed to describe the forces transmitted to the peri‐
implant‐bone interface in osseointegrated implants as well as the
effect of those forces at the implant‐bone interface and the mech‐
ano‐transduction mechanisms that guide bone‐cell interactions.
The load transferred to the implant‐bone interface is initially a
physical phenomenon, in which forces interact with the prosthetic
components, the implant body, and the surrounding bone, and de‐
formation can occur in 1 or all of the parts of the system. Once
these forces reach the bone‐implant interface, shear, bending, and
DELGADO‐RUIZ et al.
compressive moments are produced, and will impact the bone‐ma‐
trix producing stresses.
The deformations experienced by the bone matrix have different
magnitudes, are transient and multidirectional, and these charac‐
teristics produce cell reactions through mechano‐transduction pro‐
cesses. The osteocyte network receives the mechanical signal and
transmits biochemical signals to all the bone cells as a result of the
interstitial fluid movement within the canalicular system. Thus, mul‐
tiple bone‐cell interactions which are occurring at different locations
around the implant body produce and maintain the osseointegration.
The osseointegration is a dynamic process altering bone forma‐
tion and bone resorption. Within this process, ions released from
the matrix as a result of the osteoclast activity are interchanged and
incorporated into areas of bone formation because of the action of
osteoblasts, all coordinated by the osteocytes. The magnitude of
the forces acting on the bone‐implant interface, the direction of the
forces, and the period these forces are applied, will determine the
maintenance of the osseointegration equilibrium or its breakdown.
Local and individual factors can influence the strength of the
osseointegration, and therefore the biological effect of the occlusal
load (functional load or overloading) is highly variable. This might
explain the contradictory results in animal studies which attempted
to correlate implant overload with bone loss.
Further studies should be performed with the main focus on the
molecular biology of this complex phenomenon to better control
the negative effects of mechanical stresses, leading to therapy with
less risks and fewer complications. It is strongly recommended to
increase the number of studies concerning bone metabolic markers
in different loading conditions as that may help to clarify the effects
of load and overload on bone loss around osseointegrated dental
implants.
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How to cite this article: Delgado‐Ruiz RA, Calvo‐Guirado JL,
Romanos GE. Effects of occlusal forces on the peri‐implant‐
bone interface stability. Periodontol 2000. 2019;81:179–193.
https​://doi.org/10.1111/prd.12291​