The International Journal of Periodontics & Restorative Dentistry

COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE
REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
 31
REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE

Progressive Bone Adaptation of

Titanium Implants During and After
Orthodontic Load in Humans

Paolo Trisi, DDS, PhD* The use of titanium osseointegrated

Alberto Rebaudi, MD, DDS** dental implants to replace missing
teeth has been shown to be pre-
dictable1; they were first used in
The aim of the present work was the evaluation of implant stability and periim-
completely edentulous patients.2,3
plant bone reaction by histologic and clinical evaluation after therapeutic ortho-
Today, partially edentulous patients
dontic loads. Forty-one adult patients received titanium implants as an orthodon-
benefit from implant therapy. 4,5
tic anchorage device; 12 patients received a retromolar or palatal implant to
obtain tooth movement. Seven implants were removed at the end of the ortho-
Either one- or two-stage implant sys-
dontic therapy, after 2, 4, 6, and 12 months of orthodontic load, and processed tems have been documented as pro-
for histologic examination. It was possible to distalize maxillary and mandibular viding satisfactory longevity and sur-
molars and a group of teeth (molars and premolars), and to obtain tipping, vival and success rates.6,7
uprighting, intrusion, extrusion, and transfer of anchorage in other parts of the Osseointegrated implants re-
mouth. The results showed that orthodontic therapy is facilitated and quickened main stable when loaded with ortho-
by the use of implants. All implants remained stable in the bone up to 12 months dontic forces, giving the orthodon-
of loading, and all were osseointegrated. Microfractures, microcracks, and micro- tist a strong anchorage defined as
calli were observed around implants that had been placed in both low- and high- “ankylosed anchorage.” 8–12 The
density bone. The remodeling rate was still elevated after 18 months. (Int J control of anchorage is essential in
Periodontics Restorative Dent 2002;22:31–43.)
orthodontic treatment planning and
often greatly influences the objective
of therapies. Moreover, tooth move-
ments become very difficult in cir-
cumstances such as periodontally
compromised or partially edentu-
lous patients, where the remaining
teeth do not give sufficient anchor-
age. Similar problems occur when
**Private Practice, Pescara, Italy. mandibular molars or a group of
**Private Practice, Genova, Italy. teeth have to be moved distally or
vertically and when patients are
**Reprint requests: Dr Paolo Trisi, Biomaterials Clinical Research
Association, Via San Silvestro 163/3, 65132 Pescara, Italy. e-mail: unwilling to use extraoral orthodon-
paulbioc@tin.it tic devices.

Volume 22, Number 1, 2002

 32
REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE
To overcome such problems,
the use of orthodontic implants has
been studied in animals13–16 and
humans, particularly in adult ortho-
dontic treatments.17–21 There are no
standardized methods for ortho-
dontic treatments in adult pa-
tients22–24 or for orthodontic appli-
cations of implants, because few
applications have been tested.17–20
The experimental13–16 and clinical
studies17–24 showed that implants
used as orthodontic anchorage
remain stable during the traction
period, allowing orthodontic intra-
oral direct bone anchorage. Finally,
it is important to evaluate the clini-
cal improvements that can be
obtained by the use of orthodontic
implants in treatment plans.
The aim of the present article is
the evaluation, by clinical follow-up
and histologic analysis of the bone-
implant interface, of implant stabil-
ity and periimplant bone reaction
during different therapeutic ortho-
dontic conditions.
Method and materials
Orthodontic implants were manu-
factured by Exacta (Biaggini Ormco)
as a conical screw-shaped implant,
3.3 mm wide and 5 or 7 mm long
(Fig 1), made of commercially pure
titanium grade 3 (Uni 9763/2) with a
blasted surface (mean Ra = 1.329; Rt
= 21.557; Rmax = 20.847). Different
specifically designed abutments
(Biaggini Ormco) that allow several
positions of the arch were often used
to apply the orthodontic load to the
implant.
The International Journal of Periodontics & Restorative Dentistry
Patient selection and
orthodontic treatment
Forty-one adult patients needing
orthodontic treatment for various
malocclusions received titanium
implants as an orthodontic anchor-
age device. The patients received
detailed information about the aim
and scope of the therapy and
accepted the therapy.
Twenty-nine patients needed
implants as an orthodontic anchor-
age because the reduced number of
remaining teeth provided inade-
quate anchorage for orthodontic
treatment. In these patients, stan-
dard Exacta titanium-blasted
implants, 11 or 13 mm long and 4
mm in diameter, were also used as
artificial roots for the final prosthetic
rehabilitation at the end of the
orthodontic therapy. Ten patients
received a molar or retromolar
mandibular implant, and two pa-
tients received one palatal implant
each to obtain tooth movement
without compliance-dependent
anchorage aids (headgear, class II or
III elastics).21–23
Orthodontic traction was per-
formed by connecting an elastic
(Figs 2 and 3) or by placing springs
from the implants to the tooth to
be moved. One of the implants
was placed according to Roberts
et al22 in the mandibular ramus to
distalize the molars and was
immediately loaded after place-
ment using an orthodontic arch.
All other implants were loaded 2
months following placement, with
a force ranging in almost all cases
between 80 and 120 g as mea-
sured by an orthodontic dyna-
mometer.
Seven mandibular posterior
implants not useful for prosthetic
rehabilitation were removed with a
thin layer of surrounding bone and
processed for histologic examina-
tion at the end of the orthodontic
therapy. One implant was retrieved
after 2 months of load, two implants
were retrieved after 4 months of
load, one implant was retrieved after
6 months of load, and one implant
was retrieved after 12 months of
load. Two more implants had a 2-
month healing period, 8 and 6
months of loading, respectively, and
a resting period of 10 and 12
months, respectively, before re-
trieval. The overall orthodontic treat-
ment period varied from 2 to 15
months.
Surgical procedure
Exhaustive medical histories were
collected. All patients were healthy
and did not have any contraindica-
tion to oral surgical procedures.
Each patient received one or
more implants that healed nonsub-
merged. The orthoimplants were
placed 2 mm over the crestal level,
since the polished neck of the
implant measured 2 mm. Depend-
ing on the soft tissue height, a trans-
mucosal healing screw was selected
to ensure nonsubmerged healing.
The bone density was classified
using drilling resistance according
to Trisi and Rao.24
Two weeks and 1 week before
implant retrieval, the patients were

REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE
Fig 1 Implant and abutment, specifically
manufactured for orthodontic applications,
used for orthodontic anchorage.
given a single 1-g dose of tetracy-
cline (Ambramicina, Scharper) to
label the remodeling dynamics.25
After the loading period necessary
to achieve the desired tooth move-
ments, the orthoimplants were
removed. Under local anesthesia,
the orthoimplants were carefully
retrieved, together with a small por-
tion of periimplant bone, using a
cooled trephine bur. The area of
surgery was thoroughly rinsed with
sterile saline solution, and a regen-
erative procedure using a collagen
barrier membrane (Paroguide,
Vebas) was performed to obtain
healing of the residual defect.
Histologic procedure
All bone biopsies were immediately
rinsed in saline, fixed in 10% neutral
buffered formalin, and processed to
obtain thin ground sections. The
specimens were dehydrated in an
ascending series of alcohol rinses
and then embedded in Remacryl
Fig 2 In this case, orthodontic traction is
performed by connecting an elastic
between the implant abutment and the
second molar.
resin (an experimental resin, Istituto
di Microscopia Elettronica Clinica,
Ospedale Sant’Orsola). After poly-
merization, the specimens were sec-
tioned at 200 to 250 µm by a
Micromet high-speed rotating-blade
microtome (Remet) and ground
down to about 40 to 50 µm by an LS2
(Remet) grinding machine. The his-
tologic slides were stained routinely
with toluidine blue and basic fuchsin.
For the tetracycline label analysis, a
special UV filter applied to a Zeiss
Axioscop light microscope was used.
Results
The obtained tooth movements
were distalization of maxillary and
mandibular molars, contemporane-
ous distalization of a group of teeth
(molars and premolars), and tipping,
uprighting, intrusion, extrusion, and
transfer of anchorage in other parts
of the mouth.
No apparent problems occur-
red in the implants loaded with
33
Fig 3 Case from Fig 2 shows the distal-
ization of the mandibular first molar.
orthodontic force, except for one
standard 13-mm implant that
showed 4 mm of bone loss, which
healed after appropriate treatment.
No loss of bone was detectable
around the moved teeth. A com-
mon finding in standard periapical
radiographic examination of the
orthodontic implants was the appar-
ent presence of a corticalization of
the periimplant bone with forma-
tion of a radiopaque basket around
implants initially placed in low-den-
sity bone.
The movements obtained were
always very rapid compared to
movements obtained using an extra-
oral device, even when the applied
force was inferior. Some of the
implants seemed to move during
the first days of traction in the direc-
tion of the traction and to find a fixed
position after a few weeks of trac-
tion, especially when they had been
placed in very low-quality bone. All
implants healed uneventfully and
were stable until retrieval, without
signs of inflammation.
Volume 22, Number 1, 2002
 34
REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE

➔
➔
O
O

➔
➔ O

➔
* N
➔

➔
I O I
O

➔
M B I

➔
N
➔
* N

➔
➔ * ➔ N

M
* *

➔
*
* N
* *

Fig 4 Compression side of an implant
loaded for 2 months in low-density bone.
The bone showed huge resorption at the
interface (arrows). Immediately after the
resorption front, an intense intracortical
remodeling of the crest was evident, with
formation of cutting-filling cones (*) run-
ning perpendicular to the section plane
and implant surface (toluidine blue–basic
fuchsin stain; original magnification
25).
I = implant; B = bone; M = marrow spaces.
Fig 5 Buccal section of the implant in Fig
4. The bone crest shows signs of fractures
of the old bone trabeculae (arrows)
repaired by the formation of a large
amount of new woven bone (N) (toluidine
blue stain; original magnification
5). I =
implant; O = old bone.
Fig 6 Higher magnification of the thread
from Fig 5. Note the microcracks (arrows)
and newly formed bone (N) on the frac-
tured old bone (O) surfaces. Some chips of
the old bone are encased in the newly
formed bone (*) (toluidine blue stain; origi-
nal magnification
50). I = implant.

Histologic results
Two-month healing, two-month trac-
tion. This implant was oriented dur-
ing the retrieval, and it was possible
to distinguish between the different
sides during sectioning and histo-
logic analysis. A 100-g continuous
elastic traction was applied for 2
months. The implant was placed in
type II-III bone.24
The analysis of the mesiodistal
sections showed an impressive
amount of woven bone formation
at the crestal tension side and on
the apex that was positive to the
tetracycline labels. At the crest of
the compression side (Fig 4) and
the apex of the tension side, few
areas of bone-implant contact (BIC)
were visible, as the rest of the
implant was surrounded by soft tis-
sue. The thick cortical crest of the
compression side was undergoing
strong remodeling, with the for-
mation of many new cutting-filling
cones that were positive to the
double tetracycline labels running
perpendicular to the section plane
and the implant surface (Fig 4). On
this side, the bone at the interface
was undergoing huge resorption.
On the buccal aspect (Fig 5), the
bone crest showed signs of
microfractures with repairing phe-
nomena. The old, thick trabeculae of
the crest showed signs of fracture
and separation. The space between
the displaced trabeculae was filled
by newly formed lamellar or woven
bone that was labeled with double
tetracycline lines. On the middle
buccal aspect of the implant inter-
face, only newly formed composite
bone was present, directly attached
to the implant surface with small rem-
nants of fractured bone embedded
in the newly formed matrix. Also,

The International Journal of Periodontics & Restorative Dentistry


REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE
microcracks were visible at the tip of
the thread at this level (Fig 6). In
some instances, the space between
the fractured ends of the trabeculae
was quite small and was nicely filled
by new lamellar bone, with lamellae
arranged parallel to the surface of
the fractured trabeculae. In some
regions, the space between the ends
of the broken trabeculae was wider
and filled with woven bone.
Two-month healing, four-month trac-
tion. This implant was not oriented
during the retrieval, and it was not
possible to distinguish between the
different sides. An almost continuous
trabeculum layer of bone, 100 to
200 µm thick, surrounded the
implant surface (Fig 7). These tra-
beculae were thickened at three lev-
els—the crest, the threads, and the
apex—and were connected to few
thick trabeculae arranged perpen-
dicular to the implant surface. Most
of the bone matrix was made of
composite bone, with some primary
osteons at the interfacial level. A
high rate of remodeling was evident
all around the periimplant bone.
Resorption was evident at the crestal
surface, reducing the bone height
without the formation of an
infrabony pocket. The BIC seemed
very high.
Two-month healing, four-month trac-
tion. In this case, the implant and
the section were oriented. This
implant sustained a stronger force
application of 200 g 2 months before
retrieval, starting when the patient
received the double tetracycline
labeling and lasting 2 weeks. After
this strong orthodontic stress, the
force was brought back to 100 g for
the following 8 weeks before
retrieval. The pressure side showed
a huge amount of woven bone,
some still undergoing active forma-
tion and some undergoing remod-
eling (Fig 8). This bone was not in
contact with the implant surface, but
more buccally it had the aspect of a
large microcallus attached to the
implant surface on one side and con-
nected to the thin trabeculae on the
other side (Fig 9). Signs of fracture
into the trabeculae of the woven
bone in the microcallus were also
seen (Figs 10 and 11). On the tension
side, the crestal bone was fully cor-
ticalized.
The shadow of the old bone was
visible inside the crest, with a profile
that well matched that of the implant
(Fig 9) at a distance of about 1 mm
from the actual implant interface,
allowing the hypothesis of a dis-
placement of the implant in the
direction of the orthodontic traction.
This space was filled with newly
formed composite bone that was
heavily labeled with tetracycline. At
the level of the apical thread, it
seemed that the thread had
migrated from its original position,
since the imprint of the thread was
still present in the old bone even
though a remodeling process had
slightly modified this profile.
Two-month healing, six-month trac-
tion. This implant was not oriented.
Dense bone surrounded the most
coronal two thirds of the implant,
and a very dense cortex surrounded
the most coronal third (Fig 12). Bone
35
remodeling units (BRU) were visible
at this level. The surface of the crest
did not show signs of bone resorp-
tion, but areas of woven bone for-
mation were present near the
implant surface. In the central part of
the implant, the bony structures
became more cancellous. On one
side, the bone was more dense and
compact and few thick trabeculae
started from the implant surface
toward the surrounding region. The
percentage of BIC at this level was
very high. On the opposite side, the
bony structure was more cancellous,
with thin trabeculae and large mar-
row spaces, and the percentage of
BIC was low in the apical part. The
bone matrix was mainly composed
of lamellar bone.
Zero-month healing, twelve-month
traction. This implant was placed in
the very dense bone of the man-
dibular ramus. On one side, the im-
plant was surrounded only by corti-
cal bone. At this side, the most
coronal bone showed crestal growth
along the implant surface. This crest
did not show signs of resorption.
Cutting-filling cones (BRUs) were evi-
dent inside the cortical bone. Almost
all the bone matrix was composed of
lamellar bone with new osteons and
old osteons. On the opposite side,
the bone showed a reduced density
because of an intense resorption
activity that produced large marrow
spaces. Moreover, at the tip of the
screw thread, an intense remodeling
and woven bone formation was evi-
dent, as were microcracks (Fig 13). At
this side, the crest showed resorp-
tion up to the first thread.
Volume 22, Number 1, 2002
 36
REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE
S ➔
S
T M
I W
M
T M
M T
Fig 7 Four-month traction implant is sur-
rounded by cancellous bone characterized
by few thick trabeculae (T) that are fully
adherent to the implant surface, arranged
perpendicular and parallel to the implant
surface. The interfacial structure presents a
thickening of the trabeculae at three lev-
els—the crest, spire, and apex. An almost
continuous shell of bone surrounds the
implant (I), and the BIC rate is near 100%
(toluidine blue–basic fuchsin stain; original
magnification
5). S = soft connective
gingival tissues; M = marrow spaces.
The International Journal of Periodontics & Restorative Dentistry
➔ ➔
➔ ➔
* I
T C
Fig 8 Four-month traction implant. The
compression side (C) shows low-density
trabecular woven bone (W) and a low BIC
rate and almost no bone contact in the
apical part. On the tension side (T), the
bone density is high, with a thick cortical
crest (*) adherent to the implant (I); in this
part, the BIC is high (toluidine blue stain;
original magnification
5). Arrows =
direction of the orthodontic force applied.
➔
➤ N
➤
➤ T C
➤
OB
➤
➤ W
➤
➤
➤
➤
M M
Fig 9 Overview of the implant in Fig 8 in a
more lingual section. On the tension side
(T), dense bone is found. This cortical area
shows two distinct regions. At the interface,
composite bone (N) fills the space between
old mature bone (OB) and titanium surface.
A net line, matching the implant profile
(small arrowheads), delimits this front. The
profile of the implant is at a distance from
the actual interface, suggesting displace-
ment from its original position. The space
between the old bone and the actual
implant interface is filled by new woven
bone fully corticalized with new primary
osteons. Many cutting-filling cones are form-
ing inside the old bone, testifying to the
enhanced remodeling rate at this level. On
the compression side (C), woven bone struc-
tures (W) testify to the presence of a micro-
callus (large arrowheads) (toluidine blue
stain; original magnification
5). M = mar-
row space; arrows = direction of the traction.
 37
REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE

T
M

T C
C
M M
T
T

➔
T I T
I M
M
S

➔
M
➔

T S
M
M
T T
M
T
M
M

Fig 10 Higher magnification of the
implant in Fig 9 at the compression side, at
the level of the microcallus. A continuous
layer of woven bone is attached to the
implant. Many small bone trabeculae reflect
the formation of a large microcallus. A small
microcrack is visible in one of these trabecu-
lae (arrow) (toluidine blue stain; original
magnification
50). I = implant; T= woven
bone trabeculae; M = marrow spaces.
Fig 11 Higher magnification of Fig 10 at
the level of the microcallus. The arrows
point to a small microcrack in the thickness
of the woven bone trabeculae (T), proba-
bly because of the compressive forces
(toluidine blue stain; original magnification

100). M = marrow spaces.
Fig 12 Six-month traction implant. The
most coronal third is surrounded by a very
dense cortex (C). In the central part of the
implant, the bony structures become more
cancellous (S) (toluidine blue–basic fuchsin
stain; original magnification
5). M = mar-
row spaces.

Fig 13 (left) High-power magnification of

the bone-implant interface at the apex of a
thread of an implant loaded for 12 months O I
in very dense mandibular bone. S
Epifluorescent light demonstrates the S
presence of a small microcrack (arrows) of
the bone matrix aligned along the canali-
culi of the osteocytes (O), starting from the
interface (original magnification
1,000). I B
= implant; B = bone. ➔
➔ ➔ R
Fig 14 (right) Twelve-month traction, six- ➔
month rest implant. This implant was ➔ N
placed in very dense bone from the crest
➔
to the apex. On the non-remodeled side
➔
O
(N) the bone is dense, and almost 100%
BIC is evident. On the remodeled side (R)
high remodeling activity caused high
porosity and a low BIC (toluidine
blue–basic fuchsin stain; original magnifi-
cation
5). M = marrow spaces; S = soft
M
supracrestal gingival connective tissues. M

Volume 22, Number 1, 2002

 38
REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE
Two-month healing, twelve-month
traction, six-month rest. Very dense
bone from the crest to the apex sur-
rounded this implant. At the inter-
face, the bone matrix was composed
of woven bone, but many small new
BRUs were active on one side of the
implant. Because of the remodeling
spaces that induced a high porosity
of the cortical bone, the BIC was low
at this level (Fig 14) despite the cor-
ticality of the surrounding bone,
while on the opposite side the BIC
was very high and the BRU number
was lower. More bone remodeling
units were present near the interface
than at a distance. The crest did not
show any signs of resorption.
Two-month healing, eight-month
traction, ten-month rest. Very dense
cortical bone surrounded this
implant, which remained unloaded
for 10 months. The bone matrix was
mostly mature lamellar bone, with
primary and secondary osteons. The
crest showed huge resorption activ-
ity and coronal growth of the crestal
bone. Some remodeling activity was
evident, with cutting-filling cones
(BRUs) at the interface. Much higher
remodeling activity was detected
near the interface than at a distance.
The BIC was very high.
The International Journal of Periodontics & Restorative Dentistry
Discussion
According to previous re-
ports,8–12,16,21,23 implants loaded
with orthodontic appliances main-
tain osseointegration from a histo-
logic perspective; this represents an
absolute anchorage in orthodontics.
All implants in the present report
remained stable for the treatment
period. The use of rigid intraoral
anchorage units is an efficacious
alternative to orthopedic and ortho-
dontic extraoral force application
and modifies the approach to com-
plex orthodontic movements, allow-
ing simultaneous application of dif-
ferent forces in different regions of
the mouth. The force applied
through an osseointegrated implant
is continuous and allows movements
with absolute anchorage without
compliance-dependent anchorage
aids.23 It allows, for instance, the
rigid stabilization of a tooth, con-
temporaneous traction of more than
one tooth, and different three-
dimensional vector applications, by
applying all forces to a single
implant. The treatment of the pre-
sented cases was always faster than
standard treatment.
The force applied to the implant
seems to induce physiologic bone
adaptation, activating bone model-
ing and remodeling in the periim-
plant site.8 Orthodontic load is a
continuous and constant load, not
comparable to occlusal or muscular
forces. Artificial animal loading
experiments showed that static
loading has no effect on the bone
remodeling process, while dynamic
loads induce remodeling,26,27 but
other studies contradict this the-
sis.28–30 When a static load is applied
in a living subject to bone that is
also functionally loaded, this static
load is superimposed on the
dynamic strain produced by func-
tional activity. On the other hand,
experiments where long bones were
functionally isolated showed that
pure static load does not affect
remodeling, unlike dynamic
load. 31,32 In the present report,
orthodontic load was continuous,
but it was superimposed on the
dynamic strain of the basal bone
produced by physiologic functional
movements; the effect was a
dynamic periimplant bone strain.
This could explain the extensive
remodeling phenomena observed
in the periimplant bone even after
load interruption.
The histologic analysis of the
retrieved implants gave us the
unique opportunity to observe bone
adaptation patterns around implants
undergoing orthodontic load after
different loading periods, but the
number of specimens was insuffi-
cient to extrapolate statistically sig-
nificant results. Moreover, because
of the different healing times,
implant dimensions, bone densities,
and amounts and directions of
applied force, the analyzed cases
were not in comparable clinical con-
ditions.
A study in rabbits8 showed that
when the load is eccentric to the
load axis of the shaft, rapid osteo-
genesis of immature woven bone
produces a buttress-like lattice that
rapidly increases the diameter of the
shaft in the direction of concave

REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE
flexure. This process reinforces os-
seous support in a matter of days, as
revealed by tetracycline labeling.
Thus, the applied load induces rapid
osteogenesis along bone surfaces
loaded in compression as a short-
term measure to strengthen the
shaft. In the present study, the woven
bone formation was, conversely,
found inside the trabecular architec-
ture of cancellous bone. The simul-
taneous finding of microcracks and
microfractures into the thin and brit-
tle trabeculae, and the morphologic
arrangement of this woven bone,
may represent the physiologic repair
process of microfractures, “micro-
callus.”
Histologically, microcallus for-
mations consist of immature woven
bone at locally stressed sites in the
bone tissue. 33 The formation of
microcalli is a physiologic repair
mechanism of the bone tissue to sta-
bilize and renew old and brittle bone.
Even entire new trabeculae can
emerge in this way. The newly
formed woven bone trabeculae of
the microcallus are the basic prereq-
uisite for reconstruction of rarefied
bone structure.34 Although microcalli
indicate instability of the bone struc-
ture, microcallus formation stabilizes
and regenerates the bone tissue.34
Microcallus formations are demon-
strable in nearly all spongy bone by
means of suitable preparation tech-
niques. The genesis, frequency, and
importance of microcalli are largely
unknown in the orthopedic litera-
ture.34 It was postulated that trabec-
ular damage might play a role in hip
fracture, bone remodeling, and pros-
thesis loosening.35
39
The formation of microdam-
age or microscopic cracks in the
bone matrix has been associated
with elevated or altered strain envi-
ronments 36–38 and with fatigue
loading.39–42 Bone microdamage
is manifested by the presence of
well-defined microcracks in lamel-
lar bone tissue. Microcracks refers
to discrete and microscopically vis-
ible flaws that may progress and
eventually lead to a complete fail-
ure of the trabeculum. In the pre-
sent study, we found microcracks
either around implants placed in
cortical bone or in periimplant can-
cellous bone. The contemporary
presence of woven bone forma-
tion similar to microcalli substanti-
ates the occurrence of trabecular
microfractures and successive re-
pairing through microcallus forma-
tion. In our specimens, fractures of
the trabeculae and possible rela-
tive movement of the implant
could have appeared during im-
plant placement, tightening of the
abutment, or following orthodon-
tic load application.
The tetracycline labeling de-
monstrated that repair of the trabe-
cular microfractures occurred after
orthodontic load application, since
the repairing bone was labeled by
tetracycline.
It is possible that implant failure
in soft bone43,44 at the time of abut-
ment connection is due to microfrac-
turing of the thin, brittle trabeculae
of the spongious bone. In all of our
cases, no implants failed or un-
screwed during abutment connec-
tion. Nevertheless, it cannot be
excluded that microcracks without
Volume 22, Number 1, 2002
 40
REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE
implant unscrewing occurred at this
phase, since some implants were
placed in very low-density bone,
whose trabeculae are thin and brit-
tle. If this was the case, the trabecu-
lar repair should have been started
at the time of orthodontic force
application. Unfortunately, tetracy-
cline was given 2 weeks before
retrieval, so it could not label the ini-
tial phase of loading and cannot con-
firm this hypothesis.
The hypothesis of trabecular
microfractures during orthodontic
load has never been reported in the
literature, but our observations sup-
port it. In fact, two samples showed
evidence of periimplant microcalli
highly labeled later after abutment
connection, suggesting that micro-
callus formed some time after load-
ing had started.
The question of why some im-
plants present microfractures while
others do not arises. Most likely, the
difference could be a matter of bio-
mechanical load of the periimplant
bone. Among the biomechanical
parameters involved in the bone-
implant interaction are implant sur-
face and macrogeometry, bone den-
sity, amount and direction of the
applied force, early loading, and rate
of osseointegration after healing.
The rate of osseointegration for
this type of implant is high, even in
low-density bone. 45 Loading
implants after 2 months of healing
was shown to be safe 46 and is con-
sidered the standard for orthodontic
implants.9,47,48 The last factor to be
considered is the bone density.
Bone density notably varies in
the different regions of the jaws and
The International Journal of Periodontics & Restorative Dentistry
between different patients, and for
this reason it can be assumed that
implants placed in weak bony host
tissue are less resistant to biome-
chanical overstrain and are at higher
risk of failure.43,44,49 Type D4 bone
may reach up to 90% porosity.24 In
this context, it is possible to place an
implant that achieves osseointegra-
tion after an adequate healing
period, but the abrupt implant load
after the second-stage surgery may
threaten the thin and delicate bony
trabeculae attached over the implant
surface. Our observations support
this hypothesis.
In fact, histologic analysis of
implants showing microdisplace-
ment and microcalli revealed that
low-density bone surrounded them.
The occurrence of microfractures in
this context may represent one of
the mechanisms responsible for the
well-documented early postloading
failure of implants placed in low-den-
sity bone. Nevertheless, after 4
months of loading, we observed the
formation of a bone basket com-
posed of a continuous periimplant
trabeculum and few thick trabeculae
arranged at the level of the main
strain and stress force lines. Primary
osteons were appearing, giving rise
to a manifest corticalization. Some
studies8,50 showed that an ortho-
dontic load applied to an ankylosed
implant might induce bone apposi-
tion around the periimplant bone. At
6 months the bone was in a more
quiet state and the amount of BIC
was approaching 100%, but at 12
months the remodeling was still
high. In the 18-month specimens,
which had a prolonged resting
period, we expected to find a rest-
ing bone and interface, but the pat-
tern was quite similar to the 12-
month sample. The presence of
composite bone at the interface indi-
cates that the remodeling cycles had
not been able to replace all the
newly formed interfacial bone. The
presence of the woven bone could
also be explained by a possible over-
load of the periimplant bone, since
overload may induce the formation
of woven bone in critically loaded
regions.51
After 18 months, 4 to 6 52
(completed remodeling period)
were elapsed and the implant inter-
face should have reached the steady
state, but the remodeling was still
high, particularly on one side of the
implant. Previous reports8,9 showed
that the remodeling of the periim-
plant bone remains elevated
throughout the implant’s life when
implants are under functional load.
Animal studies dealing with remod-
eling of the periimplant bone sur-
rounding unloaded implants in long
bones showed a reduction of
labeled osteons at 3 months follow-
ing surgery.53 This indicates that in
the first 3 months after implantation
the high remodeling rate is mainly a
consequence of the rapid accelera-
tory phenomenon.54 Nevertheless,
in our samples, the remodeling was
also high after 6 or 10 months with-
out loading. This may be due to the
load interruption that induced disuse
atrophy, or to the disturbing effect
that the implant induces in the bio-
mechanics of the cortical bone.
On the other hand, the pres-
ence of microcracks around implants

REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE
placed in dense cortical bone, asso-
ciated with high remodeling rate and
porosity of the bone, could indicate
an overload. It has been postulated
that microdamage accumulation
stimulates remodeling, thus leading
to a net loss of bone and void for-
mation adjacent to the implant55;
this is exactly what we found around
one implant.
It has also been postulated that
bone microdamage caused by load-
ing stimulates increased new mod-
eling and remodeling events to
repair bone damage.56–58 If bone
remodeling targets bone micro-
damage for repair, and if there is a
positive feedback between damage
and remodeling, then accumulation
of microdamage around prosthetic
implants could be responsible for
the biologic responses that lead to
implant loosening.59 A recent litera-
ture review60 stated that there is evi-
dence supporting the hypothesis
that fatigue microdamage can occur
in interfacial bone around a heavily
loaded dental implant that eventu-
ally predisposes a net loss of bone
and implant failure.
Stress and strain energy is not
only proportional to the applied
force, but also to the length and
diameter of the implant, the bone
density, and the root:crown ratio. For
this reason, it is not easy to general-
ize the biologic effect observed in
the present report, but an accurate
analysis of all the biomechanical fac-
tors involved in the implant-bone
interaction is required to better
understand the biomechanical inter-
action between implant and bone
under various loading conditions.
Further studies are necessary to bet-
ter clarify these factors.
Acknowledgments
This research was supported by a grant of
the nonprofit foundation “Biomaterials
Clinical Research Association,” Pescara, Italy.
The authors wish to express their gratitude
to Dr Piero Biaggini and to Exacta (Biaggini
Ormco Italia) for providing the implant mate-
rials and supporting this work.
41
References
1. Adell R, Eriksson B, Lekholm U, Brånemark
P-I, Jemt T. Long-term follow-up study of
osseointegrated implants in the treatment
of totally edentulous jaws. Int J Oral
Maxillofac Implants 1990;5:347–359.
2. Adell R, Lekholm U, Rockler B, Brånemark
P-I. A 15-year study of osseointegrated
implants in the treatment of the edentu-
lous jaw. Int J Oral Surg 1981;10:387–416.
3. Brånemark P-I, Hansson BO, Adell R, et
al. Osseointegrated implants in the treat-
ment of the edentulous jaw. Experience
from a 10-year period. Scand J Plast
Reconstr Surg Suppl 1977;16:1–132.
4. van Steenberghe D. A retrospective mul-
ticenter evaluation of the survival rate of
osseointegrated fixtures supporting fixed
partial prostheses in the treatment of par-
tial edentulism. J Prosthet Dent 1989;61:
217–223.
5. van Steenberghe D, Lekholm U, Bolender
C, et al. Applicability of osseointegrated
oral implants in the rehabilitation of par-
tial edentulism: A prospective multicen-
ter study on 558 fixtures. Int J Oral
Maxillofac Implants 1990;5:272–281.
6. Brägger U, Hammerle C, Weber HP. Fixed
reconstructions in partially edentulous
patients using two-part ITI implants
(Bonefit) as abutments. Clin Oral Implants
Res 1990;1:41–49.
7. Buser D, Weber HP, Brägger U. The treat-
ment of partially edentulous patients with
ITI hollow-screw implants: Presurgical
evaluation and surgical procedures. Int J
Oral Maxillofac Implants 1990;5:165–175.
8. Roberts WE, Smith RK, Zilberman Y,
Mozsary PG, Smith RS. Osseous adapta-
tion to continuous loading of rigid
endosseous implants. Am J Orthod
1984;86:95–111.
9. Roberts WE, Helm FR, Marshall KJ,
Gongloff RK. Rigid endosseous implants
for orthodontic and orthopedic anchor-
age. Angle Orthod 1989;59:247–256.
10. Smalley WM, Shapiro PA, Hohl TH,
Kokich VG, Brånemark P-I. Osseointe-
grated titanium implants for maxillofacial
protraction in monkeys. Am J Orthod
Dentofac Orthop 1988;94:285–295.
Volume 22, Number 1, 2002
 42
REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE
11. Turley PK, Kean C, Schur J, et al. Ortho-
dontic force application to titanium
endosseous implants. Angle Orthod
1988;58:151–162.
12. Ödman J, Lekholm U, Jemt T, Thilander
B. Osseointegrated implants as ortho-
dontic anchorage in the treatment of par-
tially edentulous adult patients. Eur J
Orthod 1994;16:187–201.
13. Ödman J, Grondahl K, Lekholm U,
Thilander B. The effect of osseointegrat-
ed implants on the dento-alveolar devel-
opment. A clinical and radiographic study
in growing pigs. Eur J Orthod 1991;13:
279–286.
14. Thilander B, Ödman J, Grondahl K,
Lekholm U. Aspects on osseointegrated
implants inserted in growing jaws. A bio-
metric and radiographic study in the
young pig. Eur J Orthod 1992;14:99–109.
15. Sennerby L, Ödman J, Lekholm U,
Thilander B. Tissue reactions towards tita-
nium implants inserted in growing jaws.
A histological study in the pig. Clin Oral
Implants Res 1993;4:65–75.
16. Mazzocchi AR, Bernini S. Osseointe-
grated implants for maximum orthodon-
tic anchorage. J Clin Orthod 1998;7:
912–915.
17. Diedrich PR, Fuhrmann RA, Wehrbein H,
Erpenstein H. Distal movement of pre-
molars to provide posterior abutments
for missing molars. Am J Orthod
Dentofac Orthop 1996;109:355–360.
18. Higuchi KW, Slack JM. The use of titani-
um fixtures for intraoral anchorage to facil-
itate orthodontic tooth movement. Int J
Oral Maxillofac Implants 1991;6:338–344.
19. Block MS, Hoffman DR. A new device for
absolute anchorage for orthodontics. Am
J Orthod Dentofac Orthop 1995;107:
251–258.
20. Ödman J, Lekholm U, Jemt T, Brånemark
P-I, Thilander B. Osseointegrated titani-
um implants—A new approach in ortho-
dontic treatment. Eur J Orthod 1988;10:
98–105.
21. Van Roekel NB. Use of Brånemark system
implants for orthodontic anchorage:
Report of a case. Int J Oral Maxillofac
Implants 1989;4:341–344.
The International Journal of Periodontics & Restorative Dentistry
22. Roberts WE, Marshall KJ, Mozsary PG.
Rigid endosseous implant utilized as
anchorage to protract molars and close
an atrophic extraction site. Angle Orthod
1990;60:135–152.
23. Wehrbein H, Glatzmaier J, Mundwiller U,
Diedrich P. The Orthosystem—A new
implant system for orthodontic anchor-
age in the palate. J Orofac Orthop 1996;
57:142–153.
24. Trisi P, Rao W. Bone classification: Clinical-
histomorphometric comparison. Clin Oral
Implants Res 1999;10:1–7.
25. Eriksen EF, Axelrod DW, Melsen F. Bone
Histomorphometry. New York: Raven
Press, 1994.
26. Hert J, Liskova M, Landrgot B. Influence
of the long-term, continuous bending on
the bone. An experimental study on the
tibia of the rabbit. Folia Morphol (Praha)
1969;17:389–399.
27. Liskova M, Hert J. Reaction of bone to
mechanical stimuli. 2. Periosteal and
endosteal reaction of tibial diaphysis in
rabbit to intermittent loading. Folia
Morphol (Praha) 1971;19:301–317.
28. Hassler CR, Rybicki EF, Cummings KD,
Clark LC. Quantification of bone stresses
during remodeling. J Biomech 1980;13:
185–190.
29. Meade JB, Cowin SC, Klawitter JJ, Van
Buskirk WC, Skinner HB. Bone remodel-
ing due to continuously applied loads.
Calcif Tissue Int 1984;36(suppl 1):25–30.
30. Hart RT, Davy DT, Heiple KG. A compu-
tational method for stress analysis of
adaptive elastic materials with a view
toward applications in strain-induced
bone remodeling. J Biomech Eng 1984;
106:342–350.
31. Lanyon LE, Rubin CT. Static vs dynamic
loads as an influence on bone remodel-
ing. J Biomech 1984;17:897–905.
32. Rubin CT, Lanyon LE. Regulation of bone
formation by applied dynamic loads. J
Bone Joint Surg Am 1984;66:397–402.
33. Feldcamp LA, Goldstein SA, Parfitt AM,
Jesion G, Kleerekoper M. The direct
examination of three-dimensional bone
architecture in vitro by computer tomog-
raphy. J Bone Miner Res 1989;4:3–11.

REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC.PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE
34. Hahn M, Vogel M, Amling M, Ritzel H,
Delling G. Microcallus formations of the
cancellous bone: A quantitative analysis
of the human spine. J Bone Miner Res
1995;10:1410–1416.
35. Watchel EF, Keaveny TM. Dependence of
trabecular damage on mechanical strain.
J Orthop Res 1997;15:781–787.
36. Frost HM. Some ABC’s of skeletal patho-
physiology. 5. Microdamage physiology.
Calcif Tissue Int 1991;49:229–231.
37. Frost HM, Roth H, Villanueva AR. Physical
characteristics of bone. Part IV. Microsco-
pic prefailure and failure patterns. Henry
Ford Hosp Med Bull 1961;9:163–170.
38. Chamay A. Mechanical and morpholog-
ical aspects of experimental overload and
fatigue in bone. J Biomech 1970;3:
263–270.
39. Schaffler MB, Radin EL, Burr DB. Mech-
anical and morphological effects of strain
rate on fatigue of compact bone. Bone
1989;10:207–214.
40. Forwood MR, Parker AW. Microdamage
in response to repetitive torsional loading
in the rat tibia. Calcif Tissue Int 1989;45:
47–53.
41. Caler WE, Carter DR. Bone creep-fatigue
damage accumulation. J Biomech 1989;
22:625–635.
42. Carter DR, Hiyes WC. Compact bone
fatigue damage: A microscopic exami-
nation. Clin Orthop Rel Res 1977;127:
265–274.
43. Jaffin RA, Berman CL. The excessive loss
of Brånemark fixtures in type IV bone: A
5-year analysis. J Periodontol 1991;62:
2–4.
44. Bass SL, Triplett RG. The effect of preop-
erative resorption and jaw anatomy in
implant success. A report of 303 cases.
Clin Oral Implants Res 1991;2:193–198.
45. Trisi P, Rao W, Rebaudi A. A histomor-
phometric comparison of smooth and
rough titanium implants in human low-
density jaw bone. Int J Oral Maxillofac
Implants 1999;14:58–67.
43
46. Lazzara RJ, Porter SS, Testori T, Galante 58. Mori S, Burr DB. Increased intracortical
J, Zetterquist L. A prospective multicen- remodeling following fatigue damage.
ter study evaluating loading of Osseotite Bone 1993;14:103–109.
implants two months after placement: 59. Taylor M, Tanner KE. Fatigue failure of
One-year result. J Esthet Dent 1998;10: cancellous bone: A possible cause of
280–289. implant migration and loosening. J Bone
47. Linder-Aronson S, Nordenram A, Joint Surg Br 1997;79:181–182.
Anneroth G. Titanium implant anchorage 60. Brunski JB, Puleo DA, Nanci A. Biomateri-
in orthodontic treatment: An experimen- als and biomechanics of oral and max-
tal investigation in monkeys. Eur J Orthod illofacial implants: Current status and
1990;12:414–419. future developments. Int J Oral Maxillofac
48. Shapiro PA, Kokich VG. Uses of implants Implants 2000;15:15–46.
in orthodontics. Dent Clin North Am
1988;32:539–550.
49. Ulm C, Kneissel M, Schedle A, et al.
Characteristic features of trabecular bone
in edentulous maxillae. Clin Oral Implants
Res 1999;10:459–467.
50. Wehrbein H, Diedrich P. Endosseous tita-
nium implants during and after orthodon-
tic load—An experimental study in the
dog. Clin Oral Implants Res 1993;4:76–82.
51. Frost HM. Vital biomechanics of bone-
grafted dental implants. In: Jensen OT
(ed). The Sinus Bone Graft. Chicago:
Quintessence, 1999:17–25.
52. Parfitt AM. The physiologic and clinical
significance of bone histomorphometric
data. In: Recker RR (ed). Bone Histomor-
phometry: Technique and Interpretation.
Boca Raton, Fla: CRC Press, 1983:143–
223.
53. Martin RB. Osteonal remodeling in
response to screw implantation in canine
femora. J Orthop Res 1987;5:445–452.
54. Frost HM. The regional acceleratory phe-
nomenon: A review. Henry Ford Hosp
Med J 1983;31:3–9.
55. Burr DB. Microdamage in bone. Curr
Opin Orthop 1997;8:8–14.
56. Burr DB. Remodeling and the repair of
fatigue damage. Calcif Tissue Int
1993;53(suppl):75–81.
57. Hoshaw SJ, Brunski JB, Cochran GVB.
Mechanical loading of Brånemark
implants affects interfacial bone modeling
and remodeling. Int J Oral Maxillofac
Implants 1994;9:345–360.
Volume 22, Number 1, 2002