You are on page 1of 14

The International Journal of Periodontics & Restorative Dentistry

COPYRIGHT © 2005 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.
317

Peri-implant Bone Reaction to


Immediate, Early, and Delayed
Orthodontic Loading in Humans

Paolo Trisi, DDS, PhD* To achieve a predictable long-term


Alberto Rebaudi, MD, DDS** result, implants need to be in direct
contact with bone and be placed in
an adequate quality and quantity of
bone. 1–5 The research of the
Seventeen endosseous titanium implants were placed in completely edentulous
Brånemark group has demonstrated
jaws of 15 patients. The implants were loaded immediately or after 2 or 6
months, with 100 g orthodontic force. Three weeks later, the implants were over 90% long-term clinical success
removed and histologically analyzed. All of the immediately loaded implants, rates of osseointegrated dental
along with three of the eight that were loaded after 2 months, were lost. The implants in favorable sites.1 Other
remaining implants were stable until the end of the study. Histologic analysis of studies3,6–9 emphasized that the pos-
the retrieved implants showed bone remodeling in the cortical bone, thickening terior jaws are often avoided in treat-
of the bony trabeculae by new lamellar bone deposition, and microcalli of woven ment plans, because the quantity
bone or a lattice of woven bone formation around some implants that had been and quality of bone (type 4) are fre-
placed in soft bone. Tetracycline labeling revealed an elevated amount of newly quently not conducive to implant
formed bone. If further studies prove that a controlled application of orthodontic retention. In the posterior maxilla,
force, before application of occlusal loading, is able to rapidly enhance the densi-
the available bone is generally just
ty of soft peri-implant bone, we will have a powerful and precise tool to improve
sufficient for the placement of very
the rate of implant success. (Int J Periodontics Restorative Dent 2005;25:317–329.)
short implants that may be at higher
risk of failure.8,10
An implant can be clinically rigid
at the end of the healing period with
less than 25% of its surface in contact
with bone, but long-term success
cannot be expected if the biome-
chanical laws that regulate the bone
*Private Practice, Pescara, Italy; and Scientific Director of BioCRA,
Biomaterials Clinical Research Association, Pescara, Italy.
behavior at load are not respected.4
**Private Practice, Genova, Italy; and Vice President of BioCRA, In cases where bone quantity is suf-
Biomaterials Clinical Research Association, Pescara, Italy. ficient but bone quality is very low,
patients might benefit from an
Correspondence to: Dr Paolo Trisi, Biomaterials Clinical Research
Association, Via San Silvestro 163/3, 65132 Pescara, Italy. improvement of the jawbone den-
Fax: +39-085-28427. E-mail: paulbioc@tin.it sity, especially in the posterior max-

Volume 25, Number 4, 2005

COPYRIGHT © 2005 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.
318

illa and mandible. A treatment that application of a continuous load to Methods and materials
could allow a gain in the bone den- endosseous implants. In that study,
sity could improve the amount of 100-g forces were applied after 6 to Test device
bone-implant contact and the qual- 8 weeks of healing to 3.2-  8-mm
ity of bone surrounding the implant. titanium acid-etched surface im- Orthodontic implants were manu-
Currently, there are no means to plants inserted in rabbits’ femora. factured by Exacta (Biaggini Medical
predictably increase the bone den- This resulted in a rapid and impres- Devices Italia). The device is a coni-
sity in poor-quality bone during the sive increase in peri-implant bone. If cal screw-shaped implant, 3.3 mm
healing period. Nevertheless, the similarly rapid bone change could wide and 7 mm long, specifically
enhancement of bone density was be demonstrated in human jaws, it designed for orthodontic applica-
described by Frost in his “mechano- could have strong clinical implica- tions. The implants were made of
stat theory.”11–13 Frost suggested that tions for implants placed in low- commercially pure titanium grade 3
in cortical bone, when the amount of quality bone through the applica- (Uni 9763/2). The implant surface is
load exceeds a certain physiologic tion of controlled loading during the a roughened corundum-blasted sur-
threshold, bone hypertrophy results— healing period. face with a mean Ra of 1.329 (Rt =
ie, an increase in modeling and a Based on the mechanostat the- 21.557; Rmax = 20.847).
decrease in remodeling. According ory of Frost,11,13 we tried to find the
to Burr et al,14,15 bone hypertrophy is precise load that was able to induce
evoked by the application of a load a hypertrophic bone response in the Surgical procedure
able to induce a deformation of 2,500 peri-implant bone. We attempted
to 4,000 µstrain in the bone matrix. to analyze whether a similar effect Fifteen patients agreed to partici-
Published animal studies and clinical could be obtained around implants pate in the study and gave their
and histologic case reports have by applying a 100-g orthodontic informed written consent after
shown that loading over a certain load immediately after implant receiving a thorough explanation
threshold induces bone loss, while placement or after different healing about the surgical procedures. The
others contended that static loading periods in human jaws. patients included in the study
may induce corticalization.16–23 accepted the re-entry procedure to
Since bone-implant contact is a verify histologically the quality of the
static measurement that does not bone formed. The experiment was
reflect the dynamic nature of bone, performed in accordance with the
to obtain data about the dynamic Helsinki Declaration of 1975, as
changes in peri-implant bone it is revised in 1983.
necessary to label bone formation Seventeen implants were
using a double tetracycline admin- inserted in 15 adult volunteers who
istration during an experimental were undergoing a standard proce-
period.24 Specifically identifiable dure for implant placement.
bone labels are physiologic time Exhaustive medical histories were
markers. In the present study tetra- collected. All the patients were
cycline labeling of the bone was healthy and presented no con-
used to evaluate bone modeling and traindication to oral surgical proce-
remodeling around implants. dures.
A study of Roberts et al 16 The patients had to undergo
showed marked changes in bone standard implant placement in the
volume, shape, and mass following posterior jaws to replace missing

The International Journal of Periodontics & Restorative Dentistry


COPYRIGHT © 2005 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.
319

teeth. During stage-one surgery, a retrieval, the surgical site was thor- The bone histomorphometric
3.3-  7-mm implant was placed dis- oughly rinsed with sterile saline solu- parameters were calculated accord-
tal to the most distal standard tion, and a regenerative procedure ing to the standard histomorpho-
implant, in a site where the bone using a collagen barrier membrane metric technique described in the
height or quality was insufficient for was performed to help heal the literature26 and will be reported and
the placement of a standard implant. residual defect. discussed in a separate paper.
Bone density was registered by sur-
gical hand drilling resistance and
classified according to Trisi and Rao Histologic procedure
as dense, normal, or soft.25
Each patient received one or All the bone biopsy specimens were
two implants, which were loaded by immediately rinsed in saline, fixed
connecting the most distal standard in 10% neutral buffered formalin,
implant to the experimental implant and processed to obtain thin ground
via an elastic orthodontic chain sections. The specimens were dehy-
(Ormco Power Chain) that was drated in an ascending series of alco-
strained to obtain a force of 100 g hol rinses and then embedded in
lasting for 20 days, with a minimal Remacryl (an experimental resin by
reduction in strain because of the Mr Cesare Scala, Istituto di
elastic proprieties of the chain. A Microscopia Elettronica Clinica,
standard one-stage surgical tech- Ospedale Sant’Orsola). After poly-
nique was used to place implants, merization, the specimens were sec-
according to the manufacturer’s tioned to 200 to 250 µm by a
instructions. Micromet high-speed rotating blade
The patients were divided into microtome (Remet) and ground
three groups. In group A, five down to about 40 to 50 µm with an
implants were loaded immediately LS2 (Remet) grinding machine. The
after placement. In group B, eight histologic slides were stained with
implants were loaded 2 months after toluidine blue.
placement. In group C, four implants After the sectioning process was
were loaded 6 months after place- completed, each slide was analyzed
ment. During application of the histomorphometrically. This was
orthodontic load, the patients were done by digitizing the images from
instructed to take 1 g tetracycline the microscope via a JVC TK-C1380
orally on the first day of force appli- color video camera (JVC Victor
cation and 1 g of tetracycline 7 days Company) and a frame grabber. The
later.26,27 images were acquired with a 10
After 20 days of load applica- objective including the entire
tion, the experimental implants were implant surface. Subsequently, the
harvested. Under local anesthesia, digitized images were analyzed by
the experimental implants were image analysis software. For each
carefully retrieved with a low-speed implant three or more sections were
trephine bur, along with a small por- analyzed.
tion of surrounding bone. After

Volume 25, Number 4, 2005


COPYRIGHT © 2005 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.
320

Table 1 Placed (failed) implants according to healing time


and bone quality
Bone Type
Implant group Dense/normal Soft
Immediately loaded (Group A) 0 (0) 5 (5)
Loaded after 2 mo (Group B) 5 (0) 3 (3)
Loaded after 6 mo (Group C) 2 (0) 2 (0)

Fig 1 Group B implant placed in dense


cortical bone and loaded after 2 months of
healing. Numerous cutting-filling cones are
visible (arrowheads) in the cortical layer
(toluidine blue; original magnification 6).

Results the implants showed good primary in normal bone, and one in dense
stability after placement. Four bone. Two of the implants placed in
Clinical outcomes implants were lost within the first soft bone had progressively and
week of the orthodontic load, with- slowly extruded from the bone within
The overall clinical outcomes for the out clinical signs of inflammation. 2 weeks after orthodontic load appli-
experimental implants are summa- The remaining implant was lost cation and were lost without clinical
rized in Table 1. All standard within 3 weeks because of progres- signs of inflammation. One of the
implants that were connected to the sive slow extrusion, without clinical implants placed in soft bone slowly
experimental implants were clinically signs of inflammation. moved from its original position, tip-
stable and are now in clinical func- Group B implants. All the ping in the direction of the ortho-
tion and follow-up, without compli- implants loaded after 2 months (n = dontic vector during the loading
cations or detectable bone loss. 8) healed safely and appeared clini- period, and was mobile, but it was
Group A implants. The immedi- cally stable at the time of abutment still stable enough to be retrieved
ately loaded implants (n = 5) were connection. Three implants in this with the surrounding bone at the
placed in soft bone in the maxilla. All group were placed in soft bone, four defined interval. The remaining five

The International Journal of Periodontics & Restorative Dentistry


COPYRIGHT © 2005 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.
321

I
M
N
I

O N B
I O
N O M

N O

Fig 2 Group B implant placed in cortical Fig 3 In the same sample shown in Fig 2, Fig 4 Fluorescent light image of the sam-
bone and loaded after 2 months of heal- old bone surfaces (O) are covered by lay- ple shown in Fig 2. Most of the cutting-fill-
ing. Details of the intense intracortical ers of new bone (N) surrounded by large ing cones were positive to tetracycline
remodeling (arrowheads) are discernible bands of osteoid (arrowheads) (basic labels (arrow), visible as yellow lines over
by the purple staining of the newly formed fuchsin-toluidine blue; original magnifica- the black non-flourescent field (fluorescent
bone, particularly at the interface (tolui- tion 100). I = implant. light of tetracycline labeling; original magni-
dine blue and basic fuchsin; original mag- fication 50). I = implant; B = cortical bone;
nification 25). I = implant. M = marrow space.

implants placed in dense or normal Histologic results osteoid seams, and osteoblasts (Fig
bone remained stable during the 3). Most of the cutting-filling cones
loading period, without any compli- Group A implants. No histologic were positive to tetracycline labels
cations or inflammatory reactions. data were available for this group, (Fig 4), meaning they were in an
Group C implants. The implants because all the implants failed active phase at the time of tetracy-
that were loaded 6 months after place- before the established retrieval time. cline administration, ie, during load
ment (n = 4) healed safely and Group B implants. Implants application.
appeared clinically stable at the time placed in dense or normal bone Bone-resorption lacunae, con-
of abutment connection. Two implants showed the presence of a dense taining mono- or multinuclear osteo-
in this group were placed in soft bone, compact peri-implant bone layer in clasts, were found coupled in space
and two were placed in normal-density the histologic sections (Fig 1). In this and time to bone formation through
bone. All the implants in this group bone, numerous cutting-filling cones osteoid layer deposition by seams of
remained stable throughout the load- were detected (Fig 2). Moreover, the osteoblasts (Fig 5). This particular
ing period without any complications existing bone surfaces were almost process occurred in discrete remod-
or clinical inflammatory reactions. completely covered by new bone, eling sites, which were defined as

Volume 25, Number 4, 2005


COPYRIGHT © 2005 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.
322

*
T * I

⇒ T
NO
*
O
O FT
N
R R

Fig 5 Group B: 2 months of healing. Fig 6 Group C: 6 months of healing. Fig 7 Group C: 6 months of healing.
Implant placed in normal bone. Cutting- Implant placed in soft bone. In this micro- Implant placed in soft bone. In this micro-
filling cones characterized by coupled scopic field, a trabeculum (O) was sur- scopic field, a trabecular microcallus
activity of bone formation (O) and bone rounded by a thick layer of newly formed (arrow) is evident near to the implant sur-
resorption (R). A small microfracture (large bone (N), discernible by its superior stain- face (I). A fragment of old bony trabeculae
arrow) is evident near to the tip of the ing affinity (toluidine blue; original magnifi- (FT) is surrounded by newly formed woven
screw thread in an old trabeculum (T), sur- cation 50). bone (arrowheads) (toluidine blue; original
rounded by layers of newly formed bone magnification 50).
(asterisks) (toluidine blue; original magnifi-
cation 100).

bone-metabolizing units (BMUs).28,29 tissue without signs of inflammation. orthodontic loading. In these sam-
The number of the BMUs was ele- Osteoid layers were found on some ples, the bone-formation processes
vated in all samples in this group. of the peri-implant bone surfaces. were not always coupled with the
The implant placed in soft bone, Group C implants. The trabecu- resorption cavities, as in the normal
which migrated from its original posi- lae were surrounded by thick layers of remodeling processes, but the for-
tion, had a layer of dense connective newly formed bone (Fig 6), discernible mation surfaces were much more fre-
tissue surrounding most of the by its superior affinity for the stain,30 quent than the resorption surfaces.
implant interface with fibers parallel and covered by osteoid seams and In some portions of the soft
to the implant surface. A thin corti- osteoblasts. The new bone showed bone, the different staining affinity
cal shell was found outside this con- fluorescent labels, meaning they had between the old and the new bone
nective tissue layer. Islands of woven been formed during the period of and the peculiar morphology of the
bone were found in the connective tetracycline administration and hence cement lines allowed the identifica-

The International Journal of Periodontics & Restorative Dentistry


COPYRIGHT © 2005 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.
323

F
M F F M
F
F

W
Fig 9 (above) Schematic tomographic
FT three-dimensional reconstruction of a
microcallus (M) connecting the fragments
of a fractured bone trabeculum (F).
W FT
Fig 10 (above right) Schematic drawing,
based on Fig 9, showing a microcallus (M)
W between two broken ends of a fractured
trabeculum (F).

Fig 8 Higher magnification of the micro- Fig 11 Fluorescent micrograph of the


callus shown in Fig 7. The arrowheads out- section shown in Fig 8. Tetracycline label-
line the old bone fragment (FT), which is ing (arrows) is evident around the woven
surrounded by a round-shaped net of bone, which surrounds the trabecular frag-
woven bone (W) (toluidine blue; original ment (FT) outlined by small arrowheads
magnification 100). (fluorescent light, tetracycline labeling;
original magnification 100).

tion of trabecular fragments, whose labeled by tetracyclines, demon- ing was observed around all the
shapes were very similar to fractured strating that a part of it had formed implants, without distinction
bone trabeculae reported in ortho- during orthodontic load (Fig 11). between the apical and the coronal
pedic literature31 (Figs 7 and 8). In many instances the islands of regions (Fig 14).
Some of these fragments were sur- woven bone and the osteoid bands Infrabony pockets were found in
rounded by a woven bone network presented large, confluent mineral- four of the nine samples. The depth
(Figs 7 and 8), which closely resem- ization nuclei, which were a mean of of these pockets varied between 1.3
bled the aspect of a trabecular 14.44 ± 4.24 µm in diameter (Fig and 2.4 mm. The shape of these
microcallus found in fractured tra- 12). A lattice of woven bone was pockets was similar in all the cases,
beculae of the vertebrae in osteo- found in some regions around the being very narrow (300 to 500 µm)
porotic patients32,33 (Figs 9 and 10). implants that had been placed in and parallel to the implant surface,
This woven bone was partially soft bone (Fig 13). Tetracycline label- without inflammatory cells (see Fig 1).

Volume 25, Number 4, 2005


COPYRIGHT © 2005 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.
324

O C T

N I
N
B

T C

Fig 12 Group C: 6 months of healing. Fig 13 Group C: 6 months of healing. Fig 14 Same case as Fig 13. The new
Implant placed in soft bone. The osteoid Implant placed in soft bone. The trabecu- bone was always labeled by tetracycline,
layers (arrows) covering the newly formed lae were surrounded by thick layers of demonstrating that it had been formed
bone (N) were often very thick and showed newly formed bone, which is evident by during orthodontic loading. The tetracy-
large confluent “mineralization nuclei” the more intense blue staining. In this cline labeling (yellowish bands) was well
(arrowheads) contained in the large bands case, the implant was oriented to clarify diffused around the entire implant, without
of osteoid (toluidine blue; original magnifi- the difference between the compression distinction between the apical and the
cation 200). O = old bone trabeculum. (C) and tension sides (T). The large arrow- coronal regions, and at a certain distance
head indicates the direction of orthodontic from the implant surface (fluorescent light
traction. On the tension side and at the of tetracycline labels; original magnifica-
apex, a lattice of newly formed woven tion 25). I = implant; B = bone.
bone was found (arrows), while at the com-
pression side, denser bone and greater
bone-implant contact were evident. A nar-
row gap, containing vascularized fibrous
tissue without inflammatory cells, was pre-
sent at the interface on the tension side. A
small trabecular microcallus, outlined by
small arrowheads, is visible at a certain dis-
tance from the implant surface (toluidine
blue; original magnification 10).

The International Journal of Periodontics & Restorative Dentistry


COPYRIGHT © 2005 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.
325

Discussion ascribed to the better biomechani- We could suppose that the


cal competence of these implants, bone remodeling we observed
Exacta (Biaggini Medical Devices which were longer and larger than could represent an episode of RAP,
Italia) has developed an orthodontic the experimental implants. and this might be the case in the
conical screw implant, 5 to 7 mm Implants that remain stable dense peri-implant bone of the
long with a diameter of 3.3 mm, with under orthodontic force application group B implants in the present
a sandblasted titanium surface, are defined as a rigid orthodontic study. But this hypothesis may be
which has been shown to achieve a anchoring system as described in discarded for the group C samples,
high degree of osseointegration in the literature.16–18,20,35,36 Different because the RAP should end after 7
low-density human jawbone.34 bone densities have different bone to 8 weeks postimplantation38; how-
All the implants that were loaded mechanical properties and hence ever, the duration of the RAP is still
immediately after placement in soft should react differently to the same an object of discussion. Moreover,
bone were lost. On the other hand, amount of load. In dense bone we the bone-formation process seen in
three implants in the 2-month heal- observed active bone remodeling low-density bone in the present case
ing group that were placed in soft around implants that had healed for was not similar to the RAP in that it
bone were lost after 2 to 3 weeks of 2 months and were orthodontically was mediated by woven bone for-
loading. All the other implants, which loaded. This process could be a tran- mation, which is never seen in nor-
were either loaded after 2 months in sient response to the new mechani- mal remodeling processes.
denser bone or after 6 months in all cal environment induced by ortho- Another noteworthy observa-
bone qualities, remained stable until dontic loading. The end of this tion, from our histologic analysis, was
the end of the study. process will be a new arrangement the coexistence of woven bone sur-
Many variables are involved in of the peri-implant cortical rounding mature lamellar bone tra-
determining the strain induced in osteons.11–18 This was confirmed in becular fragments. These morpho-
the peri-implant bone by loading, a previous study,37 where orthodon- logic structures are quite similar to
including implant geometry, dimen- tic implants, used for clinical pur- the trabecular microcallus often
sions, position, and surface charac- poses, were histologically analyzed found in the trabecular fractures of
teristics, as well as bone density and after 6 or more months of loading. the vertebrae of osteoporotic
maturation and abutment length The regional acceleratory phe- patients.32,33 The use of tetracycline
and inclination. The results of the nomenon (RAP) described by Frost12 labeling allowed us to demonstrate
present study suggest that to sustain is common after the healing of a that this microcallus was partially
a 100-g orthodontic load, a 3.3  7- bone fracture or any other traumatic formed during orthodontic load
mm implant placed in poor-quality injury to the bone and represents a application.
bone requires a healing period localized remodeling event through Fractured trabeculae may
longer than 2 months. According to the bone adjacent to any invasive undergo repair through the
the results of the present study, the bone procedure. The process ends for mation of a microcallus. 32
application of a similar force without with the restoration of the normal Histologically, microcallus forma-
waiting for a 6-month healing period bone structure. This process is char- tions consist of immature woven
in soft bone, led to the loosening of acterized by resorption coupled with bone and are formed at locally
the implants and hence to implant formation of new functionally ori- stressed sites in the bone tissue.39,40
failure due to overload. ented bone. Surgical implantation of The formation of microcalli is a
All the standard implants con- a screw is among the stimuli resulting physiologic repair mechanism of
nected to the experimental implants in a RAP.38 A key feature of a RAP is the trabecular bone to stabilize and
performed clinically well and are still a pro tempore increase in activation renew old and brittle bone. Entire
in clinical function. This may be of osteonal remodeling foci.38 new trabeculae can emerge in this

Volume 25, Number 4, 2005


COPYRIGHT © 2005 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.
326

way. The newly formed woven bone Soft bone may reach up to 90%
trabeculae of the microcallus are a porosity.25 In this context, the place-
basic prerequisite for reconstruc- ment of an implant is possible, but a
tion of rarefied bone structure.39,40 sudden onset of loading, commonly
Although microcalli can indicate performed after second-stage
instability of a bone structure, surgery, may threaten the thin and
microcallus formation is not only a delicate bone trabeculae at the
negative mechanism, but stabilizes implant surface. If the peri-implant
and regenerates the bone tis- bone is not strong enough to stabi-
sue.39,40 Microcallus formations are lize the loaded implant, trabecular
demonstrable in nearly all spongy bone fractures will occur, inducing
bone by means of suitable prepa- the failure of the implant itself. This
ration techniques. The genesis, fre- could explain the failures observed
quency, and importance of micro- in the present cases involving soft
calli are largely unknown in the bone. This observation could be in
orthopedic and dental literature. It accordance with the study of Melsen
was postulated that trabecular and Lang,23 who observed in a finite
damage might play a role in hip element analysis that not all force
fracture, bone remodeling, and systems may be tolerated on a long-
prosthesis loosening.39,40 term basis by the peri-implant bone.
The formation of microdamage High strain values (above 6,700
or microscopic cracks in the bone µstrain) resulted in a high incidence
matrix has been associated with ele- of resorption and negative balance
vated or altered strain environ- between bone apposition and bone
ments41,42 and with fatigue load- resorption. Isidor47 observed pre-
ing.43–46 It was hypothesized that sumptive failure of implants as a
trabecular fractures were caused by result of overload, which he
the orthodontic load application, but explained as the inability of bone to
this hypothesis was discarded, since repair microfractures developed as a
the microcalli were partially pre- result of excessive occlusal loading.
existing before orthodontic load, as In these kinds of clinical situa-
evidenced by the partial labeling by tions, any tools able to rapidly
tetracycline. The trabecular fractures enhance the bone density, particu-
were likely caused by bone drilling larly at the interface, may be helpful
during implant site preparation or to improve the implant survival rate.
by implant placement or abutment The enhancement of bone density
connection. The new labeled bone was described by Frost11–13 in his
formed around the microcallus could mechanostat theory. In the present
be the expression of the normal study, the thickening of the bone
healing process of trabecular frac- trabeculae observed in the 6-month
tures. samples could represent a hyper-
It is common knowledge that trophic response to the load, as pre-
implants placed in low-quality bone dicted by the mechanostat the-
are at a higher risk of failure.7,8,23,37 ory. 11–13 Tetracycline labeling

The International Journal of Periodontics & Restorative Dentistry


COPYRIGHT © 2005 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.
327

allowed us to determine that the to form “calcifying nodules” is the


thickening of the bony trabeculae consequence of accretion of calcium
started exactly at the time of the and phosphorus ions by epitaxy.
load application and proceeded for Additional deposition of crystalline
all of the loading period, since the mineral results in the fusion of nod-
distance between the two tetracy- ules into the calcifying front
cline labels corresponded to the proper.48–50 The normal diameter of
bone formed between the two these calcifying nodules is between
administrations of labels. 1 and 2 µm. In the present observa-
Previous studies have shown tions, these nodules were much
that orthodontic loading induces larger (around 14 µm). The reason for
corticalization in the peri-implant this could be twofold: an increase in
bone.22,23,37 We speculate that in the bone formation rate and/or a
the present study, the end result of decrease in mineralization leg time.
the observed phenomenon could Further studies are needed to
have been a net augmentation of verify that controlled orthodontic
the peri-implant bone structure. We force application, before occlusal
also observed an increase in the load application, can rapidly
thickness of the osteoid bands and enhance the peri-implant bone den-
the mineralization nuclei, also called sity in soft bone. If proven, clinicians
“nodular calcifications,” “large will have a powerful and precise tool
aggregates of mineral material,” to improve implant success rates.
“calcified micro-spheres,” or “calci- Further studies are needed to better
fied nodules”; these are normally clarify the effects of controlled ortho-
found in the osteoid of healthy dontic load in human jawbone.
patients.48–50 Although the under-
standing of the process of primary
mineralization is not complete, there Acknowledgments
is broad consensus regarding the
role of matrix vesicles in the onset of The authors wish to express their gratitude
to Dr Piero Biaggini and to Exacta (Biaggini
extracellular matrix mineralization. Medical Devices) for providing the implant
These mineralizaton nuclei were pre- materials and for partially supporting this
viously observed and described, but work. This research was supported by a grant
from the nonprofit foundation “Biomaterials
were of a different diameter com-
Clinical Research Association,” Pescara, Italy.
pared with our observation.48,50 This
trilaminar membrane, invested with
organelles 0.05 to 0.25 µm in diam-
eter, originates from the forming
cells and appears in the matrix
loaded with calcium-phosphate. The
appearance of apatite crystals within
the vesicles is followed by rupture of
their membranes. Further growth of
the crystals and their accumulation

Volume 25, Number 4, 2005


COPYRIGHT © 2005 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.
328

References 12. Frost HM. The regional acceleratory phe- 23. Melsen B, Lang NP. Biological reactions
nomenon: A review. Henry Ford Hosp of alveolar bone to orthodontic loading
Med J 1983;31:3–9. of oral implants. Clin Oral Implants Res
1. Adell R, Lekholm U, Rockler B, Brånemark
13. Frost HM. The skeletal intermediary orga- 2001;12:144–152.
P-l. A 15-year study of osseointegrated
implants in the treatment of the edentu- nization. Metab Bone Dis Relat Res 24. Garretto LP, Chen J, Parr JA, Roberts WE.
lous jaw. Int J Oral Surg 1981;10:387–416. 1983;4:281–290. Remodeling dynamics of bone support-
14. Burr DB, Schamer MB, Yang KH, et al. ing rigidly fixed titanium implants: A his-
2. Adell R, Eriksson B, Lekholm U,
Skeletal change in response to altered tomorphometric comparison in four
Brånemark P-I, Jemt T. Long-term follow-
strain environments: Is woven bone a species including humans. Implant Dent
up study of osseointegrated implants in
response to elevated strain? Bone 1995;4:235–243.
the treatment of totally edentulous jaws.
Int J Oral Maxillofac Implants 1990;3: 1989;10:223–233. 25. Trisi P, Rao W. Bone classification: Clinical-
347–359. 15. Burr DB, Schamer MB, Yang KH, et al. The histomorphometric comparison. Clin Oral
effects of altered strain environments on Implants Res 1999;10:1–7.
3. Jemt T, Lekholm U, Adell R.
Osseointegrated implants in the treat- bone tissue kinetics. Bone 1989;10: 26. Recker RR. Bone histomorphometry:
ment of partially edentulous patients: A 215–221. Techniques and interpretation. Boca
preliminary study on 876 consecutively 16. Roberts WE, Smith RK, Zilberman Y, Raton, FL: CRC Press, 1983.
placed fixtures. Int J Oral Maxillofac Mozsary PG, Smith RS. Osseous adapta- 27. Frost HM. Bone histomorphometry:
Implants 1989;4:211–17. tion to continuous loading of rigid Choice of marking agent and labeling
4. Misch CE. Contemporary Implant endosseous implants. Am J Orthod schedule. In: Recker RR (ed). Bone
Dentistry. St Louis: Mosby, 1993. 1984;86:95–111. Histomorphometry: Techniques and
17. Roberts WE, Helm FR, Marshall KJ, Interpretation. Boca Raton, FL: CRC
5. Misch CE. Factors involved in dental
Gongloff RK. Rigid endosseous implants Press, 1983:38–52.
implant abutments. J Mich Dent Assoc
1987;69:149–151. for orthodontic and orthopedic anchor- 28. Frost HM. Relation between bone tissue
age. Angle Orthod 1989;59:247–256. and cell population dynamics, histology
6. Jemt T, Lekholm U. Oral implant treat-
18. Roberts WE, Simmons KE, Garetto LP, and tetracycline labeling. Clin Orthop
ment in posterior partially edentulous
DeCastro RA. Bone physiology and 1966;49:65–75.
jaws: A 5-year follow-up report. Int J Oral
Maxillofac Implants 1993;8:635–640. metabolism in dental implantology: Risk 29. Frost HM. Tetracycline-based histological
factors for osteoporosis and other meta- analysis of bone remodeling. Calcif Tissue
7. Jamn RA, Berman CL. The excessive loss
bolic bone diseases. Implant Dent Res 1969;3:211–237.
of Brånemark fixtures in type IV bone: A
1992;1:11–21.
5-year analysis. J Periodontol 1991;62: 30. Schenk RK. Cytodynamics and histody-
2–4. 19. Wehrbein H, Diedrich P. Endosseous tita- namics of primary bone repair. In: Lane
nium implants during and after ortho- JM (ed). Fracture Healing. New York:
8. Block MS, Gardiner D, Kent JN, Misiek DJ,
dontic load—An experimental study in Churchill Livingstone, 1987:23–32.
Finger IM, Guerra L. Hydroxyapatite-coat-
the dog. Clin Oral Implants Res 1993;
ed cylindrical implants in the posterior 31. Schenk RK. Biology of fracture repair. In:
4:76–82.
mandible: 10-year observations. Int J Oral Browner BD, Jupiter JB, Levine AM,
Maxillofac lmplants 1996;11:626–633. 20. Wehrbein H. Endosseous titanium Trafton PG (eds). Skeletal Trauma.
implants as orthodontic anchoring ele- Philadelphia: Saunders, 1992:31–76.
9. Nevins M, Langer B. The successful appli-
ments. Experimental studies and clinical
cation of osseointegrated implants to the 32. Mosekilde L. The effect of modeling and
application. Fortschr Kieferorthop
posterior jaw: A long-term retrospective remodeling on human vertebral body
1994;55:236–250.
study. Int J Oral Maxillofac Implants architecture. Technol Health Care
1993;8:428–432. 21. Wehrbein H, Merz BR, Hammerle CH, 1998;6:287–297.
Lang NP. Bone-to-implant contact of
10. Wheeler SL. Eight-year clinical retro- 33. Mosekilde L. Consequences of the
orthodontic implants in humans subject-
spective study of titanium plasma- remodelling process for vertebral tra-
ed to horizontal loading. Clin Oral
sprayed and hydroxyapatite-coated cylin- becular bone structure: A scanning elec-
Implants Res 1998;9:348–353.
der implants. Int J Oral Maxillofac tron microscopy study (uncoupling of
lmplants 1996;11:340–350. 22. Gotfredsen K, Berglundh T, Lindhe J. unloaded structures). Bone Miner
Bone reactions adjacent to titanium 1990;10:13–35.
11. Frost HM. A determinant of bone archi-
implants subjected to static load. A study
tecture. The minimum effective strain. 34. Trisi P, Rao W, Rebaudi A. A histometric
in the dog (I). Clin Oral Implants Res
Clin Orthop 1983;May:286–292. comparison of smooth and rough titani-
2001;12:1–8.
um implants in human low-density jaw-
bone. Int J Oral Maxillofac lmplants
1999;14:689–698.

The International Journal of Periodontics & Restorative Dentistry


COPYRIGHT © 2005 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.
329

35. Turley PK, Kean C, Schur J, et al. 48. Anderson HC. Calcium-accumulating
Orthodontic force application to titani- vesicles in the intercellular matrix of bone.
um endosseous implants. Angle Orthod In: CIBA Foundation Symposium 11 (ed).
1988;58:151–162. Hard tissue growth, repair and reminer-
36. Wehrbein H, Glatzmaier J, Mundwiller U, alization. Amsterdam 1973:213–216.
Diedrich P. The Orthosystem—A new 49. Sela J, Bab IA. The mechanism of prima-
implant system for orthodontic anchor- ry mineralization in the reaction of bone
age in the palate. J Orofac Orthop to injury and administration of implant. J
1996;57:142–153. Biomed Mater Res 1985;19:225–231.
37. Trisi P, Rebaudi A. Progressive bone adap- 50. Aaron JE, Oliver B, Clarke N, Carter DH.
tation of titanium implants during and Calcified microspheres as biological enti-
after orthodontic load in humans. Int J ties and their isolation from bone.
Periodontics Restorative Dent 2002;22: Histochem J 1999;31:455–470.
31–43.
38. Martin RB. Osteonal remodeling in
response to screw implantation in canine
femora. J Orthop Res 1987;5:445–452.
39. Hahn M, Vogel M, Amling M, et al. Micro-
callus formation of spongiosa. An up to
now underestimated repair mechanism of
the skeletal system. Pathologie 1994;
15:297–302.
40. 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.
41. Frost HM. Some ABC’s of skeletal patho-
physiology. 5. Microdamage physiology.
Calcif Tissue Int 1991;49:229–231.
42. Chamay A. Mechanical and morpholog-
ical aspects of experimental overload and
fatigue in bone. J Biomech 1970;3:
263–270.
43. Schamer MB, Radin EL, Burr DB.
Mechanical and morphological effects of
strain rate on fatigue of compact bone.
Bone 1989;10:207–214.
44. Forwood MR, Parker AW. Microdamage
in response to repetitive torsional loading
in the rat tibia. Calcif Tissue Int 1989;45:
47–53.
45. Caler WE, Carter DR. Bone creep-fatigue
damage accumulation. J Biomech 1989;
22:625–635.
46. Carter DR, Hayes WC. Compact bone
fatigue damage: A microscopic exami-
nation. Clin Orthop 1977;(127):265–274.
47. Isidor F. Loss of osseointegration caused
by occlusal load of oral implants. A clini-
cal and radiographic study in monkeys.
Clin Oral Implants Res 1996;7:143–152.

Volume 25, Number 4, 2005


COPYRIGHT © 2005 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.

You might also like