De novo alveolar bone formation adjacent to endosseous ......De novo alveolar bone formation...

De novo alveolar bone formationadjacent to endosseous implantsA model study in the dog

Tord BerglundhIngemar AbrahamssonNiklaus P. LangJan Lindhe

Authors’ affiliations:Tord Berglundh, Ingemar Abrahamsson,Jan Lindhe, Goteborg University, SwedenNiklaus P. Lang, University of Berne, Switzerland

Correspondence to:Prof. O. D. Tord BerglundhDepartment of Periodontology,The Sahlgrenska Academy at Goteborg University,Box 450 S-405 30 GoteborgSwedenFax þ 46 31 773 3791e-mail: [email protected]

Key words: experimental model, initial bone formation, in vivo, osseointegration, wound

healing

Abstract:

Objective: To describe a model for the investigation of different phases of wound healing

that are involved in the process resulting in osseointegration.

Material and methods: The implants used for the study of early healing had a geometry that

corresponded to that of a solid screw implant with an SLA surface configuration. A

circumferential trough had been prepared within the thread region (intra-osseous portion)

that established a geometrically well-defined wound compartment. Twenty Labrador dogs

received 160 experimental devices totally to allow the evaluation of healing between 2h

and 12 weeks. Both ground sections and decalcified sections were prepared from different

implant sites.

Results: The experimental chamber used appeared to be conducive for the study of early

phases of bone formation. The ground sections provided an overview of the various phases

of soft and hard tissue formation, while the decalcified, thin sections enabled a more

detailed study of events involved in bone tissue modeling and remodeling. The initially

emptywound chamber became occupiedwith a coagulum and a granulation tissue that was

replaced by a provisional matrix. The process of bone formation started already during the

first week. The newly formed bone present at the lateral border of the cut bony bed

appeared to be continuous with the parent bone, but woven bone was also found on the

SLA surface at a distance from the parent bone. This primary bone that included trabeculae

of woven bonewas replaced by parallel-fibered and/or lamellar bone andmarrow. Between

1 and 2 weeks, the bone tissue immediately lateral to the pitch region, responsible for

primary mechanical stability of the device, became resorbed and replaced with newly

formed viable bone. Despite this temporary loss of hard tissue contact, the implants

remained clinically stable at all times.

Conclusion: Osseointegration represents a dynamic process both during its establishment

and its maintenance. In the establishment phase, there is a delicate interplay between bone

resorption in contact regions (between the titanium body and mineralized bone) and bone

formation in ‘contact- free’ areas. During the maintenance phase, osseointegration is

secured through continuous remodeling and adaptation to function.

The healing of oral implants (made of

c.p. titanium) into the jawbone is

based on osseointegration or ‘functional

ankylosis’ as described by Branemark et al.

(1969) and Schroeder et al. (1976). This

principle originally called for healing

periods of several months and was aimed

at the establishment of a direct bone-

to-implant contact that, according to

definition, must be documented by

means of histology. The prerequisites for

osseointegration included (1) infliction of

minimal trauma during surgery, (2) estab-

lishment of primary implant stability andISSN 0905-7161

Copyright r Blackwell Munksgaard 2003

Date:Accepted 19 December 2002

To cite this article:Berglundh T, Abrahamsson I, Lang NP,Lindhe J. De novo alveolar bone formation adjacent toendosseous implants. A model study in the dog.Clin Oral Impl Res, 14, 2003, 251–262

251

(3) avoidance of infection and micromotion

during healing.

Recently, shorter healing periods were

advocated for some implant systems, thus

allowing shorter rehabilitation periods

for the patient (Cochran et al. 2002). It

has even been suggested that immediate

loading of endosseous implants may be a

realistic treatment alternative in various

jawbone regions (Glauser et al. 2001).

Installation of implants in the alveolar

process elicits a sequence of healing events

including necrosis and subsequent resorp-

tion of traumatized bone around the tita-

nium body concomitant with new bone

formation. While the implant displays

initial mechanical stability due to contact

and friction between the implant surface

and the severed bone, the long-term main-

tenance of implant stability calls for a

biologic attachment between the foreign

body and the surrounding tissue.

However, short-term clinical studies

provided some evidence that immediate

loading of installed implants may, indeed,

be successful (Glauser et al. 2001). Limited

information is available on the predictabil-

ity of practising such treatment protocols.

It is, therefore, of utmost importance to

identify the biological sequences of healing

during the early phases of tissue integration

when the primary mechanical stability of

the implant has to be substituted with stabi-

lity obtained through biological means.

The objective of the present report was

to describe a novel model to investigate

different phases of wound healing that

are involved in the process that results in

osseointegration.

Material and methods

The device

The implants used for the study of early

healing had a geometry that corresponded

to that of the solid screw implant of the

ITIs Dental Implant System (Institute

Straumann AG, Waldenburg, Switzerland).

The device was made from c.p. titanium

(grade IV) and had an outer diameter of

4.1 mm. The intraosseous part of the

implant was 10 mm in length and was

configured with a turned or SLA-surface

topography. In the current report the data

presentation will be restricted to implants

with the SLA surface.

As for the original ITIs Dental Implant

System, the distance between the pitch of

the thread was 1.25 mm. However, with

the exception of the marginal 1-mm area, a

0.40-mm deep U-shaped circumferential

trough had been prepared within the thread

region (intraosseous portion), but leaving

the tip of each pitch untouched (Fig. 1).

Hereby, a secluded area, an experimental

wound chamber, was created following

implant installation.

In a longitudinal cross-section of the

experimental device (Fig. 2), various land-

marks of the chamber were identified: (a)

the two pitches that constituted the outer

delineation of the chamber and (b) the inner

U-shaped walls.

Following implant installation the

pitches engaged the hard tissue walls of

the cylindrical canal prepared in the jaw-

bone and provided primary mechanical

stability of the device. The inner portion

of the chamber thus established a geome-

trically well-defined wound compartment.

Experimental animals

The study protocol was approved by the

regional Ethics Committee for Animal

Research, Gothenburg, Sweden. Twenty

Labrador dogs were included in the experi-

ment. All mandibular premolars were

extracted. After a healing period of 3

months, the staggered implant installation

procedure outlined in Table 1 was initiated.

Thus, buccal and lingual soft tissue flaps

were elevated and four of the devices were

placed in the right side of the mandible (R1,

R2, R3 and R4) in all 20 dogs (Fig. 3).

The bone tissue at the experimental sites

was prepared for implant installation ac-

cording to directions given in the manual of

the implant system. A nonsubmerged

implant installation technique was used

and the mucosal tissues were secured to the

inverse conical, polished marginal portion

of the device with interrupted sutures. The

sutures were removed after 2 weeks, and a

plaque control program including daily

cleaning of the remaining teeth and the

implants was initiated.

Implant installation was subsequently

performed in the left side of the mandible

(L1, L2, L3 and L4) according to the

schedule outlined in Table 1.

The animals were sacrificed and biopsies

were obtained at various intervals to pro-

vide healing periods extending from Day 0

(2 h) to 12 weeks (Table 1). At each biopsy

interval, the animals were sacrificed with

Fig. 1. Experimental implant device: screw-shaped

titanium implant, diameter 4.1 mm, length 10 mm

with circumferential trough in the endosseous part.

1.25 mm

0.40 mm

aa

b

aa

0.35 mm

Fig. 2. Cross-section of the wound chambers pro-

vided by the device: a, pitches engaging the bone

tissue walls; b, inner U-shaped wound chamber

proper. The dotted line indicates the lateral wall of

the chamber, i.e. the position of the cut bone surface.

Berglundh et al . De novo bone formation

252 | Clin. Oral Impl. Res. 14, 2003 / 251–262

an overdose of sodium-Pentothals and

perfused through the carotid arteries by

a fixative (Karnovsky 1965). The mand-

ibles were removed and placed in the

fixative. The implant sites were dissected

using a diamond saw (Exakts, Kulzer,

Germany) and processed for histological

analysis.

Histological preparation and analysis

Decalcified sections

Two of the implant sites in each quadrant

were prepared using a modification of

the ‘fracture technique’ described by

Berglundh et al. (1991, 1994). Before the

tissue was fully decalcified, incisions were

made parallel with the long axis of the

implants and at the mesial and distal

aspects of the biopsies. Buccal and lingual

portions of the peri-implant tissues were

carefully dissected and one mesio-buccal,

one mesio-lingual, one disto-buccal and

one disto-lingual unit prepared. Decalcifi-

cation was completed in EDTA and dehy-

dration performed in serial steps of ethanol

concentrations. Secondary fixation in

OsO4 of the tissue samples was carried

out and the units were finally embedded in

EPONs (Schroeder 1969). Sections were

produced from each tissue unit with

the microtome set at 3 mm. The sections

were stained in PAS and toluidine blue

(Schroeder 1969). From each tissue

unit, six selected sections representing

the entire circumference (mesio-buccal,

mesio-lingual, disto-buccal, disto-lingual)

of the implant were exposed to histological

examination.

Nondecalcified sections

In the remaining four sites of each animal,

ground sections were prepared according to

methods described by Donath & Breuner

(1982). The blocks were cut in a bucco-

lingual plane using a cutting-grinding unit

(Exakts, Apparatebau, Norderstedt, Ger-

many). From each implant site, two central

sections were obtained and further reduced

to a final thickness of about 20mm by

microgrinding and polishing using a micro-

grinding unit (Exakts, Apparatebau, Nor-

derstedt, Germany). The remaining mesial

and distal portions were cut in a perpendi-

cular (mesial–distal) direction and two cen-

tral sections were prepared from each unit.

The sections were stained in toluidine blue.

Histological analysis

The histological examination was per-

formed in a Leitz DM-RBEs microscope

(Leica, Heidelberg, Germany) equipped

with an image system (Q-500 MCs; Leica,

Heidelberg, Germany). Digital micrographs

were obtained using a digital camera (DC

200; Leica, Heidelberg, Germany) con-

nected to the microscope.

Results

Healing was uneventful following device

installation in all 20 dogs and for all 160

implant sites. No implant exhibited clin-

ical mobility. Further, the mucosa exhib-

ited only minor signs of inflammation

during the first few weeks of healing, and

no infection arose during the observation

intervals at any implant site.

Day 0 (2 h)

Fig. 4a–c illustrates a cross-section (ground

section) of an implant with surrounding

Table 1. Schedule for implant installation and biopsy; each group (I–IV) included five animals

Day 0 Day 4 Week 1 Week 2 Week 4 Week 6 Week 8 Week 12

LeftGroup I

InstallationBiopsy

Right Installation

LeftGroup II

InstallationBiopsy

Right Installation

LeftGroup III

InstallationBiopsy

Right Installation

LeftGroup IV

InstallationBiopsy

Right Installation

Fig. 3. Placement of experimental devices: three devices installed and one in the process of being installed.

Berglundh et al . De novo bone formation 1


soft and hard tissues from a biopsy sampled

2 h after the end of surgical installation.

The peripheral portions of the pitches of the

thread were in close contact with the

surrounding bone tissue, and thus hereby

mechanical stability for the implant during

the initial phase of wound healing was

provided (Fig. 4b; arrows). The experimen-

tal chamber units of the device were

occupied with a coagulum. In decalcified

sections (Fig. 4c), the various cells within

this coagulum could be identified. Thus,

large numbers of erythrocytes, as well as

some neutrophils and macrophages, oc-

curred within a network of fibrin (Fig. 4d).

Day 4

Fig. 5a (ground section) illustrates a device

with the soft and hard tissues that were

present in a biopsy obtained from the 4-day

interval of healing. Within the experimen-

tal chamber units, the coagulum had

apparently been replaced with a tissue

(Fig. 5b) that was characterized by the

occurrence of a multitude of ‘fibroblast-

like’ cells (mesenchymal cells) which

surrounded vascular structures (Fig. 6a,b).

In the newly formed tissue immediately

lateral to the titanium surface, the densely

c d

a b

Fig. 4. (a) Device with surrounding soft and hard tissues sampled 2 h after installation. Ground section. Original mag: � 16. Wound chambers created between the pitches

of the thread. Inset: (b) Pitches (arrows) in close contact with the bone tissue. Wound chamber filled with coagulum. Ground section. Original mag. � 50. (c) Wound

chamber with coagulum 2 h after device installation. Decalcified section. Original mag. � 100 Inset: Fig. 4d. (d) Coagulum including large numbers of erythrocytes and

some inflammatory cells. Original mag. � 400.



packed cells resided in a stroma of fibrin-

like structures. In this area of the chamber,

only few inflammatory cells could be seen

(Fig. 6b), while in more central portions of

the chamber region several inflammatory

cells occurred around vascular structures in

the newly formed soft tissue (Fig. 7).

Osteoclasts were found on the cut bone

surface.

1 week

In biopsies obtained after 1 week, the

chambers of the experimental device ap-

peared to be occupied with a provisional

matrix, part of which contained areas of

newly formed woven bone (Fig. 8; ground

section) The provisional matrix was rich in

collagen fibrils and sprouting vascular

structures surrounded by scattered inflam-

matory cells. Areas of a newly formed bone

could be observed around most of the

vascular units (Fig. 9a,b; decalcified sec-

tion). Portions of the newly formed bone

also appeared to be in direct contact with

the SLA surface. The trabeculae of woven

bone were lined with osteoblasts; and

osteocytes were found within the newly

formed bone tissue.

2 weeks

After 2 weeks of wound healing, new bone

formation appeared to be intense in all

compartments surrounding the device

(Fig. 10; ground section). Large areas of

woven bone were also present in the bone

marrow regions ‘apical’ to the implant.

The newly formed bone extended from

the surface of the parent bone into the

chamber (Fig. 11). This newly formed bone

was seen to occupy almost all surface

regions of the device (Fig. 12).

The bone tissue next to the implant wall

was lined with osteoblasts that were facing

a provisional matrix that was rich in

vascular units, spindle-shaped cells, few

leukocytes and collagen fibrils (Fig. 13a–c).

In the center of the chamber, the

connective tissue was characterized by the

a b

Fig. 5. (a) Device with soft and hard tissues representing 4 days of healing. Ground section. Original mag. � 16.

Inset: Fig. 5b. (b) Wound chamber filled with a tissue in close contact with the SLA surface. Ground section.

Original mag. � 100.

a b

Fig. 6. (a) Wound chamber at 4 days. Decalcified section. Original mag. �200. Tissue rich in vascular structures. (b) Wound chamber at 4 days of healing. Decalcified

section. Original mag. � 400. Within the newly formed tissue, densely packed connective tissue cells are trapped in an organic stroma. Some inflammatory cells adjacent

to the vasculature.



presence of large amounts of vascular

structures, many of which presented with

a wide lumen. Spindle-shaped cells and

collagen fibrils with a haphazard orienta-

tion surrounded the vasculature (Fig. 13c).

The trabeculae of woven bone were lined

by bone-forming cells (osteoblasts) indi-

cating that, in most areas of the experi-

mental chamber, bone formation was in

progress.

In some pitch regions of the device,

i.e. in areas that were responsible for

primary mechanical stability, the bone

tissue exhibited signs of ongoing bone

remodeling, resorption and apposition.

Note the areas of new bone formation

lateral to the ‘pitch’ regions in Fig. 14

(ground section).

4 weeks

After 4 weeks following device installation

(Fig. 15a–c), wound healing continued to be

characterized by the marked formation of

new bone. This newly formed mineralized

tissue extended from the cut bone surface

into the chamber, but projected also along

the SLA surface of the chamber. The

central portion of the experimental cham-

ber was filled with a primary spongiosa

that was rich in vascular structures and

various morphotypes of fibroblast-like

cells. The newly formed bone included

woven bone often combined with both

parallel-fibered and lamellar bone. In

the pitch regions, the bone remodeling

appeared to be intense.

6, 8 and 12 weeks

After 6 weeks of healing, most of the

experimental chambers appeared to be

filled with bone (Fig. 16a). The tissue that

extended from the parent bone had the

character of woven bone or parallel-fibered

and lamellar bone. Large areas of this newly

formed bone were characterized by the

occurrence of primary and secondary os-

teons, and such mineralized tissues were

also in close contact with the implant

surface. After 8 and 12 weeks (Fig. 16b,

c), marked signs of remodeling could

be seen in the bone tissue occupying the

experimental chamber. This hard tissue

was surrounded by a bone marrow contain-

ing adipocytes, vessels, collagen fibers and

some mononuclear leukocytes.

Fig. 7. Wound chamber at 4 days. Decalcified section. Original mag.�400. Large number of cells and vascular

structures.

Fig. 8. Wound chamber after 1 week. Ground section. Original mag. � 40. First sign of bone formation. Primary

spongiosa including trabeculae and woven bone present around the vascular units and also on the SLA chamber

surface (‘Osteo-coating’).



Discussion

The experimental chamber used in the

current model experiment appeared to be

conducive for the study of early phases of

bone formation. The ground sections pro-

vided an overview of the various phases of

soft and hard tissue formation, while the

decalcified, thin sections enabled a more

detailed study of events involved in bone

tissue modeling and remodeling.

The initially empty wound chamber

became occupied with a coagulum and a

granulation tissue that, within a few days,

was replaced by a provisional matrix:

connective tissue including large numbers

of mesenchymal cells embedded in a

fibrous matrix (Cardaropoli et al. 2003).

The process of bone formation started

already during the first week of wound

healing. The newly formed bone present at

the lateral border of the cut bony bed

appeared to be continuous with the parent

bone (appositional bone formation or dis-

tance osteogenesis; Davies 1998), but

woven bone was also found on the SLA

surface at a distance from the parent bone of

the implant site (contact osteogenesis;

Davies 1998). This primary bone spongiosa

or ‘primary spongework’ (Schenk 1994)

that included trabeculae of woven bone

was, during the subsequent weeks, replaced

with more mature bone tissue, i.e. parallel-

fibered and/or lamellar bone and marrow.

In some respect, the observations of the

current experimental model were in agree-

ment with the findings reported by Sen-

nerby et al. (1993), who studied ‘early

tissue response to titanium implants in-

serted in rabbit bone’.

a b

Fig. 9. (a) Wound chamber after 1 week. Decalcified section. Original mag. � 200. Woven bone penetrating most of the chamber volume and also occurring on the SLA

chamber surface (arrows). Inset: Fig. 9b. (b) Osteoblasts lining the bone trabeculae and osteocytes found within the newly formed bone. Original mag. �400.

Fig. 10. Device with surrounding tissues after 2 weeks of healing. Ground section. Original mag. � 16. Presence

of large volumes of woven bone in the tissues surrounding the device. Inset: Fig. 11.



Thus, these authors concluded that the

insertion of titanium implants into the

rabbit tibia within the first 3 days induced

migration of mesenchymal cells into the

defect and that the first signs of hard tissue

formation could be seen after 1 week. The

authors further stated that immature wo-

ven bone started to fill the threads from the

seventh day and this bone was remodeled to

lamellar bone. This process was completed

6 weeks to 3 months after the insertion of

the implants. However, in variance with

the results of the present study, the authors

failed to demonstrate the occurrence of an

early direct bone formation on the implant

surface. The reason for this discrepancy

may be explained by the fact that, while in

the current experiment the device was

designed with a rough SLA surface, the

implants used by Sennerby et al. (1993) had

a turned or machined surface. The signifi-

cance of implant microtopography in opti-

mizing osseointegration was discussed by

e.g. Wennerberg et al. (1995), Cochran et al.

(1998), Davies (1998) and Abrahamsson

et al. (2001). They concluded that a rough-

ened in comparison to a turned surface

will enhance ‘osteoconduction’ and conse-

quently improve the implant integration.

The patterns of bone formation observed

in the current model are also consistent

with previous descriptions of bone model-

ing and remodeling in bone defects of

varying locations and dimensions, e.g.

extraction sockets (Amler 1969, Cardaro-

poli et al. 2003), furcation defects (Araujo

et al. 1997, 1998), in membrane-protected

bone augmentation (Kostopoulos & Kar-

ring 1994, Kostopoulos et al. 1994, Ham-

merle et al. 1996) or in defects in the

alveolar bone (e.g. Schenk et al. 1994,

Botticelli et al. 2003a,b). In comparing

such studies, it should be realized, how-

ever, that the size and configuration of the

wound, the defect, to undergo bone model-

ing and remodeling will influence the rate

of completion of the healing process (Lang

et al. 1994). The advantage of the model

used in the present investigation is its close

resemblance to the clinical situation, i.e.

when a screw-shaped implant is installed in

an edentulous ridge. Therefore, based on

the current data, there are reasons to

assume that the formation of mineralized

bone occurs very early on and adjacent to

the implant following its installation. To

what extent the surface configuration and

Fig. 11. Wound chamber. Original mag. � 100. Contains newly formed mineralized tissue (dark stain)

continuous with the parent bone and along the SLA chamber surface. Arrows indicate areas of remodeling in the

parent bone.

Fig. 12. Detail of Fig. 11. Original mag. � 200. Woven bone contains osteocytes and trabeculae are lined with

osteoblasts. Note the early development of primary osteons (arrows).



geometry of the implant influence wound

healing that results in bone formation can

easily be studied in the standardized cham-

bers of the device used in the present

model. Furthermore, the model appears

conducive for the study of the influence

on bone formation of e.g. occlusal forces

leading to micromotion as a sequellae of

immediate and early loading.

During the surgical site preparation in

the current model, the cylindrical bed in

the alveolar bone was finally tapped using a

standard device of the ITIs Dental Implant

System. As a result, only light torque forces

were required during installation of the

device. Hence, it can be assumed that only

a minimal pressure was exerted to the

lateral bony walls of the implant bed at

the pitch region.

Between the 1- and 4-week interval of

wound healing, the bone tissue immedi-

ately lateral to the pitch region, responsible

for primary mechanical stability of the

device, became resorbed in discrete areas

(Fig. 14) and replaced with newly formed

viable bone. Despite this temporary loss of

hard tissue contact, the implants remained

clinically stable at all times. This, in turn,

means that already during the first weeks of

healing, the mechanical anchorage of the

implant in the current model must have

been replaced with a biological attachment

including de novo formation of a primary

spongework (Schenk 1994) that included

the establishment of woven bone on the

surface of the titanium device. It was

evident that during later phases of healing,

remodeling occurred that improved the

quality of the hard tissue attachment both

with respect to its mechanical and meta-

bolic properties (Schenk 1994).

The current findings indicate clearly that

osseointegration represents a dynamic pro-

cess both during its establishment and its

maintenance. In the establishment phase,

there is a delicate interplay between bone

resorption in contact regions between the

a b c

Fig. 13. (a) Wound chamber representing 2 weeks of healing. Decalcified section. Original mag. � 100. Mineralized bone coating the entire SLA chamber surface. (b)

Detail of Fig. (a). Original mag. � 200. Woven bone continuous with parent bone (appositional bone formation), but newly formed bone also present on the SLA surface in

areas remote of the parent bone (Contact osteogenesis). (c) Detail of Fig. 13(b). Original mag. � 400. Spindle-shaped cells and collagen fibrils present around the

vasculature.

Fig. 14. Bone remodeling in a pitch region 2 weeks after device installation. Ground section. Original mag.

�200. New bone has formed to re-establish bone- to- implant contact in the pitch region.



titanium body and mineralized bone, and

bone formation in ‘contact-free’ areas. Dur-

ing the maintenance phase, osseointegration

is secured through continuous remodeling

and adaptation to function (Wolff 1892).

It can be argued that the establishment

phase of osseointegration is relatively

short for an implant that, following instal-

lation, yields a large contact-free surface

compared to an implant with a large

contact surface. Obviously, the magnitude

of the press-fit and the resulting bone

necrosis may also influence the rate of

osseointegration.

Acknowledgment This project was

supported by a Research Program

Project grant (179/2000) from the ITI

Foundation for the Promotion of Oral

Implantology, Switzerland.

Resume

Objetivo: Describir un modelo para la investigacion

de las diferentes fases de cicatrizacion osea que

estan involucrados en el proceso que resulta en la

osteointegracion.

Material y metodos: Los implantes usados para el

estudio de cicatrizacion temprana tenıan una geo-

metrıa que se correspondıa con la de un implante con

configuracion de tornillo macizo con una superficie

SLA. Se preparo una circunferencia completa dentro

de la region de la rosca (porcion intraosea) que

establecio un compartimiento de herida geometrica-

mente bien definido. 20 perros Labrador recibieron

160 dispositivos experimentales para permitir la

evaluacion de la cicatrizacion entre 2 horas y 12

semanas. Se prepararon secciones base y descalcifi-

cadas de diferentes lugares de implantes.

Resultados: La camara experimental usada parecio

ser conductiva para el estudio de las fases tempranas

de la formacion osea. Las secciones base suminis-

traron una perspectiva de las varias fases de la

formacion de tejido blando y duro, mientras que las

secciones delgadas, descalcificadas permitieron un

estudio mas detallado de los eventos involucrados en

el modelaje y remodelaje del tejido oseo.

a b c

Fig. 15. (a) Wound chamber representing 4 weeks of healing. Ground section. Mag. � 50. The dark stained areas indicate newly formed bone that extends from the cut

bone surface into the chamber. Inset Fig. 15 b and 15 c. (b) Detail of Fig. 15(a). (original mag. � 100). Portions of the mineralized part of the primary spongiosa are in

apparent contact with the SLA surface. (c) Pitch region of the chamber border (original mag. � 100). The remodeling activity is marked in areas both adjacent to the pitch

and within the parent bone.

a b c

Fig. 16. (a) Wound chamber representing 6 weeks of healing. Decalcified section; original mag. � 200. The tissue within the chamber is comprised of a mix of woven bone,

parallel-fibered and lamellar bone. (b,c) After 8 weeks (b) and 12 weeks (c) the chamber is occupied with mature bone and includes also areas of bone marrow in contact with

the SLA surface (ground section; original mag. �100).



La camara de la herida inicialmente vacıa se ocupo

con un coagulo y un tejido de granulacion que fue

sustituido por una matriz provisional. El proceso de

formacion de hueso comenzo ya durante la primera

semana. El hueso neoformado presente en el borde

lateral del corte del lecho oseo parecio ser continuo

con el hueso matriz, pero tambien se encontro hueso

inmaduro en la superficie SLA a distancia del hueso

matriz. Este hueso primario que incluyo trabeculas

de hueso inmaduro fue sustituido por hueso de fibras

paralelas y/o lamelar y medula. Entre una y dos

semanas, el tejido oseo inmediatamente lateral a la

zona basal, responsable de la estabilidad mecanica

primaria del dispositivo, fue reabsorbida y reempla-

zada con hueso neoformado viable. A pesar de esta

perdida temporal de contacto con tejido duro, los

implantes permanecieron clınicamente estables todo

el tiempo.

Conclusion: La osteointegracion representa un

proceso dinamico durante su establecimiento y su

mantenimiento. En la fase de establecimiento, existe

una delicada interaccion entre reabsorcion osea en las

regiones de contacto (entre el cuerpo de titanio y el

hueso mineralizado) y la formacion osea en la areas

‘‘libres de contacto’’. Durante la fase de manteni-

miento, la osteointegracion esta asegurada a traves de

remodelado continuo y adaptacion a la funcion.

Zusammenfassung

Ziel: - die Beschreibung eines Modells zur Untersu-

chung der verschiedenen Phasen der Wundheilung,

welche am Prozess der Osseointegration beteiligt

sind.

Material und Methoden: Die Implantate, welche fur

die Studie der fruhen Heilungsprozesse verwendet

wurden, wiesen eine Geometrie auf, welche der

eines Vollschraubenimplantats mit SLA-Oberflache

entsprach. Rund um die Implantate wurde im

Bereich des Gewindes eine Kerbe prapariert (intra-

ossarer Anteil), welche ein geometrisch gut defi-

niertes Wundkompartiment abgrenzte. 20 Labrador-

hunde erhielten insgesamt 160 experimentelle

Implantate, um die Heilungsprozesse zwischen 2

Stunden und 12 Wochen zu untersuchen. Von den

verschiedenen Implantatstellen wurden sowohl

Schliffpraparate als auch dekalzifizierte Schnittpra-

parate hergestellt.

Resultate: Die experimentelle Kammer schein

geeignet fur die Untersuchung der ersten Phase der

Knochenformation zu sein. Die Schliffpraparate

lieferten eine Uebersicht uber die verschiednen

Phasen der Weich- und Hartgewebsheilung, wah-

rend die dekalzifizierten dunnen Schnittpraparate

eine genauere Untersuchung der Ablaufe bei der

Knochengewebsbildung und beim Knochenumbau

erlaubten.

Die anfanglich leere Wundkammer wurde mit

einem Koagulum und Granulationsgewebe aufge-

fullt, welches durch eine provisorische Matrix

ersetzt wurde. Der Prozess der Knochenbildung

begann bereits wahrend der ersten Woche. Der neu

gebildete Knochen im Bereich der lateralen Grenze

des geschnittenen Knochenbetts schien in Zusam-

menhang mit dem ortstandigen Knochen zu sein,

aber Geflechtknochen konnte auch auf der SLA-

Oberflache mit einer gewissen Distanz zum

ortstandigen Knochen gefunden werden. Dieser

primare Knochen, welcher Trabekel aus Geflecht-

knochen beinhaltete, wurde durch parallelfaserigen

und/oder lamellaren Knochen und Knochenmark

ersetzt. Zwischen einer und zwei Wochen wurde das

Knochengewebe, welches unmittelbar lateral der

Kante des Gewindes lag und verantwortlich fur die

primare mechanische Stabilitat des Implantats ist,

resorbiert und durch neu gebildeten vitalen Knochen

ersetzt. Trotz dieses temporaren Kontaktverlustes

mit dem Hartgewebe blieben die Implantate zu

jedem Zeitpunkt klinisch stabil.

Schlussfolgerung: Die Osseointegration stellt wah-

rend der Bildung und wahrend des Erhalts einen

dynamischen Prozess dar. In der Bildungsphase

besteht ein empfindliches Wechselspiel zwischen

der Knochenresorption in der Kontaktregion

(zwischen dem Titankorper und dem mineralisierten

Knochen) und der Knochenbildung in der ‘‘kontakt-

freien’’ Zone. Wahrend der Erhaltungsphase wird die

Osseointegration durch standige Umbauvorgange

und funktionelle Adaptation gesichert.

Resumen

Este estudio se llevo a cabo para comparar la

exactitud de la determinacion del contorno mandib-

ular y la posicion del canal mandibular en mandıbu-

las de cadaver por medio del metodo de

reconstruccion multiplanar (MPR-CT), que recien-

temente se ha convertido de uso extendido para

examenes preoperatorios, con aquellas tecnicas

tomograficas y para evaluar la utilidad de MPR-CT.

Se escanearon un total de 6 lugares en la region molar

de 3 mandıbulas de cadaver usando tres sistemas de

imagenes, i.e. escaner Quantum CT, Scanora y OP-

100. Las imagenes obtenidas se midieron dos veces

cada una por 4 radiologos. Las estructuras anatomi-

cas medidas fueron altura y grosor de la mandıbula,

distancia de la cresta alveolar al canal mandibular, y

distancia desde el hueso cortical vestibular al canal

mandibular. Tras realizar el escaner, las areas

escaneadas de las mandıbulas se cortaron en lonchas

de 2 mm de grosor, y se obtuvieron imagenes

radiologicas blandas de estos cortes. Los valores

de las ya mencionadas 4 estructuras anatomicas

obtenidas por mediciones en los radiogramas radio-

graficos usando calibres de visualizacion digital se

consideraron como valores reales, los errores en la

distancia desde la cresta alveolar al canal mandibular

estaban dentro de 1 mm (±1 mm) en 93.7% de las

mediciones por CT-directa, 89.6% de las mediciones

por MPR_CT, 87.5% de las mediciones por Scanora,

y el 47.9% de las mediciones por OP-100, y la

exactitud de los 4 metodos se clasificaron en orden de

CT-directa, MPR-CT, MPR-CT, Scanora, y OP-100.

Se observo una tendencia similar en las medi-

ciones de otras estructuras anatomicas, y se obser-

varon diferencias estadısticamente significativas

entre los metodos. De este modo, MPR-CT permite

unas mediciones mas exactas que las de las otras 2

tecnicas tomograficas, y ser util como examen

preoperatorio para cirugıa de implantes.

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