Journal of Cranio-Maxillofacial Surgery (2008) 36, 21e27

Ó 2007 European Association for Cranio-Maxillofacial Surgery

doi:10.1016/j.jcms.2007.07.006, available online at http://www.sciencedirect.com

Primary loading of palatal implants for orthodontic anchorage e

A pilot animal study

Péter BORBÉLY1, Miklós P. DUNAY2, Britta A. JUNG3, Heinrich WEHRBEIN3,

Wilfried WAGNER4, Martin KUNKEL4
1
Fogszabályozási Stúdió, Private Practice, Budapest, Hungary; 2 Department of Surgery (Chair: Prof. Dr. Tibor
Nemeth) Szent István University, Faculty of Veterinary Science, Budapest, Hungary; 3 Department of
Orthodontics (Chair: Prof. Dr. Dr. H. Wehrbein); 4 Department of Oral and Maxillofacial Surgery
(Chair: Prof. Dr. Dr. W. Wagner) University of Mainz, Germany

SUMMARY. Objectives: This study aimed at evaluating the clinical performance and osseointegration of short
orthodontic implants immediately loaded with orthodontic forces. Material and methods: The investigation
was designed as an experimental animal study. Eight palatal implants of the Ortho-systemÒ were immediately
loaded with 100 cN after palatal insertion in 4 female german shepherd dogs. Xylene orange and calcein green
were used for polychrome sequential labelling. Histological preparation utilized the cutting and grinding tech-
nique. Outcome variables were clinical implant success, histological osseointegration and bone-to-implant con-
tact rates. Results: All (8/8) implants were clinically successful and stable when the animals were sacrificed.
One implant showed fibrous encapsulation and was histologically classified as ‘‘failed’’ for ‘‘osseointegration’’.
Upon morphometrical analysis, bone to implant contact rates for newly formed or remodelled bone were 19%
at 4 weeks and 26% at 6 months. The fluorochrome labelling indicated substantial mineral apposition on the sur-
face of the implants at the end of the first and the second postoperative months. Conclusion: This study re-
vealed borderline reliability of osseointegration for immediately loaded palatal implants but reasonable bone
formation at the 4th postoperative week. Thus, two clinical concepts are both supported: early orthodontic load-
ing after 4 weeks as well as improvement of primary stability to provide a biomechanical basis for immediate or-
thodontic loading. Ó 2007 European Association for Cranio-Maxillofacial Surgery

Keywords: palatal implant, Ortho-systemÒ, Ortho implantÒ, orthodontic loading, osseointegration, dental
implants, animal study, polychrome sequential labelling, orthodontic anchorage, early loading, morphometry

INTRODUCTION introduced for orthodontic loading in the last decade.

Anchorage, defined as the ‘‘resistance to unwanted
tooth movement’’ is a fundamental orthodontic problem
and a major determinant of success in the treatment of
dental and skeletal dysgnathia (Diedrich, 1993; Willems
et al., 1999). Loading of an anchorage unit in orthodontic
treatment is possible on the conditions of a static equilib-
rium of forces (action ¼ reaction). Hence, if teeth are
used for anchorage, their reaction to quantity, type and
duration of the forces and moments applied through the
orthodontic biomechanics is critical for active movement
of other teeth. Anchorage can be enhanced to a limited
degree by connecting several teeth using rigid steel wires
or heavy ligatures. Supportive appliances such as ‘‘exter-
nal’’ headgear and inter-maxillary elastics can provide
additional stability. However, these pose considerable
inconveniences, are visible, and even bear the risk of
potential injury (Booth-Mason and Birnie, 1988; Blum-
Hareuveni et al., 2004). Moreover, patients acceptance
is crucial and compliance is another limiting factor
(Diedrich, 1993).
To overcome the limits of dental orthodontic anchor-
age, numerous skeletal anchorage devices have been
Today, there is evidence, that osseointegrated implants
remain positionally stable under typical orthodontic load-
ing conditions (Wehrbein & Diedrich, 1993; Wehrbein
et al., 1996a, 1996b, 1999; Bernhart et al., 2001; Freu-
denthaler et al., 2001; Fortini et al., 2004).
The use of palatal implants of the Ortho-systemÒ (Strau-
mann, Basel, Switzerland) has been extensively investi-
gated and can be regarded as a classic for orthodontic
skeletal anchorage (Wehrbein & Diedrich, 1993; Wehr-
bein, 1994; Wehrbein et al., 1996a, 1996b, 1998, 1999;
Cously, 2005). However, a relevant drawback of this sys-
tem is, at least according to the present manufacturers in-
structions, that the healing period has to be at least
3 months.
Encouraged by recent research progress in implantol-
ogy (Cochran et al., 2004; Nkenke and Fenner, 2006)
demonstrating high success rates for immediate and early
loading in prosthetic implants, it was the aim of this pilot
study to evaluate, whether immediate loading could also
be applied for short orthodontic implants. Therefore, an
experimental animal study was initiated, to investigate
the feasibility of immediate loading for palatal implants
of the OrthoÒ- system.

21
22 Journal of Cranio-Maxillofacial Surgery
MATERIAL AND METHODS
Animals
Four female german shepherd dogs (age 1 year) were op-
erated upon under general anaesthesia. The study proto-
col was approved by the review board of the Hungarian

Ministry of Agriculture (Ref. Nr. FTv. Aeü. 
és Éell. All.
271/2003/2004).
Following sedation by subcutaneous application of
0.1 mg/kg (body weight) acepromazine (Vetranquil 1%:
Ceva-Sante Animale, La Ballastiere, France), the animals
were anaesthesized by an intra-venous bolus of xylazine
(Primazin 2%: Alfasan International, Woerden, Nether-
lands) 1 mg/kg and ketamine (Calypsol: Richter,
Budapest, Hungary) 10 mg/kg. For peri-operative prophy-
laxis the animals received 30 mg/kg amoxicillin and
7.5 mg/kg clavulanic acid (Synulox RTU: Pfizer, Sand-
wich, UK). Prior to intraoral surgery, a polividone iodine
mouth-rinse (Betadine: Egis, Budapest, Hungary) was
applied for local disinfection. Meloxicam 0.2 mg/kg
(Metacam 0.5%: Labania Life Science, Barcelona, Spain)
was given subcutaneously for peri- and post-operative
analgesia.
Palatal implants of the Ortho-systemÒ (Straumann,
Basel, Germany) of 3.36 mm with a sandblasted large
grit acid etched (SLA) surface were inserted according
to the manufacturers instructions in the midsagittal plane
at the depression of the 3rd and 5th palatal mucosal fold,
corresponding to the position of 1st and 3rd premolars.
This was chosen to ensure minimal per-implant thickness
of palatal mucosa. Briefly, the palatal mucosa was re-
moved at the prospective site of implant placement
with a rotating mucosal trephine. Using a round bur,
a slight bony indentation was created in the midline.
Thereafter the implant site was prepared using the
OrthoÒ profile drill to a depth of 6 mm. All drilling pro-
cedures were performed under copious irrigation with
sterile physiological saline. Then the implants were in-
serted using the appropriate ratchet. All implants were
clinically stable at the time of insertion.
Steel tubes soldered to steel OrthoÒ-caps served as
attachments for coil springs. The OrthoÒ-caps were in-
serted and fixation screws were placed using cyanoacry-
late glue (Loctite 496, Loctite, Munich, Germany) to
protect the screws from loosening. For immediate load-
ing, NieTi coil springs of 100 cN were placed between
the implants and fixed with 0.3 mm stainless steel wires
(Fig. 1). To prevent soft tissue irritation due to sharp
edges, wires and tubes were encapsulated by using
a light-cured orthodontic adhesive (TransbondTM XT,
3M-Unitek, Puchheim, Germany). Lateral and axial ra-
diographic checks were performed immediately after im-
plant placement and at the time of harvesting the
specimens. The animals were kept on a strict soft diet
(Pedigree Adult for Medium Dogs, Masterfood, Cson-
grad, Hungary) with water ad libitum.
For polychrome sequential labelling, two substances
were administered: 15 mg/kg calceine green: 1% buff-
ered in hydrogen carbonate solution 2% after the first
post-operative week, 90 mg/kg xylene orange: 6%
buffered in hydrogen carbonate solution 2% after the
Fig. 1 e Palatal implants immediately postoperately. Coil-spring
attached to small tubes soldered to OrthoÒ-caps. Light curing resin
added later. Inset: lateral view of the implants after harvesting and
sectioning the maxilla.
first post-operative month and again 15 mg/kg calceine
green: 1% buffered in hydrogen carbonate solution 2%
after the second post-operative month.
Specimens and histological processing
After 4 weeks 2 dogs and after 6 months the other 2 dogs
were sacrificed. The maxillae were dissected out and
fixed by immersion in 50% ethanol for 10 days. For his-
tological preparation, the cutting and grinding technique
according to Donath and Breuner (1982) was used. In
brief, after fixation, the bones were immersed into as-
cending concentrations up to absolute ethanol over 2
weeks and then embedded in a mixture of glycol methac-
rylate (Technovit 7200 VLCÒ, Kulzer, Wehrheim, Ger-
many). Polymerisation was obtained by light curing
with a light source of 450 nm wave length. From each
specimen, sections were cut in the sagittal plane parallel
to the implant’s longitudinal axis, using a diamond band
saw. This allowed for the definition of implant surface
orientation as either in the direction of the force or oppo-
site to the force direction. Thereafter, the sections were
ground and polished on a micro-grinding system (EX-
ACT, Norderstedt, Germany) to a final thickness of
20 mm. The sections were stained by haematoxylin/eosin
for light microscopy after fluorescence microscopy.
Evaluation of stained sections
All histological examinations were performed on a
LeicaÒ DM/RBE microscope equipped with the digital
image system IM50Ò. To evaluate the bone-to-implant
contact rate, the contour of each implant was scanned
by a series of microphotographs (Matrix 25601920)
with an original magnification of 100. The entire im-
plant surface was displayed by merging these 14e18 dig-
ital images. For morphometrical analysis, a grid of 50 mm
was placed over the implant. Thus the surface was repre-
sented by 339e416 fields of 50 mm50 mm per implant.

Each field was classified according to one of the follow-
ing four categories:
d Fibrous connective tissue or bone marrow,
d Bony debris,
d Primary bone-to-implant contact: bone without signs
of remodelling,
d Secondary bone-to-implant contact: newly formed or
remodelled bone.
The rate of primary-to-secondary contact was calcu-
lated as the proportion of fields showing direct bone
contact for the complete surface of the implant. In addi-
tion, the same was listed for both implant sides, the im-
plant side in the direction of and the one opposite to the
force direction. All results were given as the percentage
of bone contact divided by the total whole implant surface.
Statistical analysis
Until now, success criteria as used in dental implantology
have not been established in the field of orthodontic an-
chorage devices. Thus two endpoints were defined in or-
der to measure success or failure of the implants. The
primary endpoint was ‘‘clinical stability’’. An implant
was classified as clinically stable, if there was no loss
of the implant under orthodontic loading. The second
endpoint was ‘‘osseointegration’’. In this pilot study,
gross fibrous encapsulation and a bone to implant
contact of less than 10% was considered as a failure.
According to these definitions, success rates are given
separately for each of the two endpoints.
The bone-to-implant contact rates were compared for
the implants retrieved at 4 weeks and at 6 months using
the non-parametric U-Test for independent samples ac-
cording to Mann and Whitney. To compare the bone-
to-implant contact rates of the traction (opposite to force
direction) and the pressure sides (in force direction) of
the implant, the Wilcoxon test for paired samples was ap-
plied. For graphic description, box plots are given. All
calculations were carried out using SPSS for Windows,
Version 11 (SPSS Inc., Chicago, USA).
RESULTS
Clinical implant success
The implants, OrthoÒ-caps and the coil springs were well
tolerated by the animals. Except for the symptomless
loosening of the covering resin in 1 animal, the
orthodontic loading set-up was kept for the duration of
the study in all animals. All implants of this series (8
out of 8) remained clinically stable under constant linear
loading conditions with 100 cN for 4 weeks and for 6
Table 1 e Implant success and bone-to-implant contact rates
Time of evaluation Implants clinically
stable
4 weeks 4 out of 4
6 months 4 out of 4
* Failed implant excluded.
Primary loading of palatal implants 23
months. At the time when the animals were sacrificed,
there was no exposure of the implants on the side of
the nasal cavity (Table 1).
Upon histological evaluation, however 1 implant (ante-
rior implant, 6 months animal) showed almost complete
fibrous encapsulation with only minimal bone-to-implant
contact of less than 4%. This implant was classified as
‘‘failed’’ for the endpoint ‘‘osseointegration’’.
Histological evaluation of osseointegration
After 4 weeks, all 4 implant sites showed considerable de-
posits of bony debris (12e23% of the implant surface) re-
sulting from the drilling and insertion procedure (Fig. 2).
However, all implants had zones of primary bone contact
without apparent signs of remodelling (12e21%; mean
16% (^5) of the implant surface). Besides this, the spec-
imens showed distinct sites of new bone formation either
as pseudopodial and finger-like contacts or as linear bone
formation along the implant surface. In these areas, cover-
ing 6e29% (mean 19% ^12) of the implant surface,
high-power magnification (1000) displayed osteocytes
in close vicinity to the implant surface (Fig. 3).
After 6 months of implant loading, complete remodel-
ling has taken place (primary bone contact \2%) and the
deposits of abraded, non-vital bone had vanished. The
overall secondary bone to implant contact ratio remained
at a rather low level (mean 20% (^13) with one (ante-
rior) implant being almost completely encapsulated by
fibrous tissue (Fig. 4). Excluding this implant whose
osseointegration was classified as ‘‘failed’’, the mean
overall bone-to-implant contact rate of the 3 osseointe-
grated implants was 26% (^9). Although the immediate
Fig. 2 e Specimen harvested after 4 weeks. Substantial deposits of
bony debris (deep blue) discernible along the implants surface (HE;
100).
Implants Primary bone to Secondary bone to
osseointegrated implant contact implants contact
4 out of 4 16% (^5) 19% (^12)
3 out of 4 2% (^3) 26% (^9)*
24 Journal of Cranio-Maxillofacial Surgery
bone-to-implant contacts were still predominantly of
a pseudopodial type with numerous gaps and extended
zones of fibrous tissue, the surrounding bone appeared
condensed with only few marrow spaces remaining. In
Figure 4, the bone to implant contact zones are high-
lighted in green for the specimens of a 6 months animal
in which one implant was histologically classified as
a failure. Only punctate contacts remained in this failed
anterior implant, whilst there was about 34% bone-to-
implant contact rate in the successful posterior implant
of this animal.
The box plots in Fig. 5 represent the primary and sec-
ondary bone contact rates at 4 weeks and at 6 months. In
spite of a moderate increase of the secondary bone con-
Fig. 3 e Detail of the new bone found after 4 weeks. Osteocytes (/)
of typical morphology in close contact to the implant surface (HE;
1000).
Fig. 4 e Bone to implant contacts in a ‘‘failed’’ (A: animal 3, anterior) and a ‘‘successful’’ (B: animal 3, posterior) implant (HE; original magnification
100; 17(in A)/14 (in B) microphotographs merged). Actual contact zones, evaluated in increments of 50 mm, are highlighted in green.
tact rate, there was no significant difference of bone con-
tact between the specimens retrieved at 4 weeks when
compared with the 6 months group (p ¼ 0.343;
ManneWhitney U-Test, n.s.; Table 1). There was no sig-
nificant difference between the ‘‘traction’’ and the ‘‘pres-
sure’’ side of the implants (p ¼ 0.345e0.889; Wilcoxon
matched pairs test) regarding the bone to implant contact
rates.
Polychrome sequential labelling
In the specimens retrieved after 4 weeks, the first calcein-
green labelling, administered at postoperative day 7, re-
sulted in only diffuse green fluorescence at the sites of
abraded bone chips displaced into marrow spaces and to-
wards the tip of the implants. There was only minor la-
belling of the bone in the immediate vicinity of the
surface of the implant at this time. The intense green
fluorescence in Fig. 6 (/) represents such a zone of
bony debris. Comparably minor bone apposition (i.e.
fluorochrome marking) could be detected close to a thread
in this specimen (*).
In the 6 months specimens the diffuse fluorescence
areas of the first dose of calcein-green had completely
vanished. The fluorochromes administered after the first
and second post-operative months were easily identified
as well-defined fluorescent bands. At this time, fluoro-
chrome incorporation was mainly seen in the surround-
ing bone and only to a minor extent at the immediate
surface of the implants (Figs 7a and b).
DISCUSSION
In the last few years, a large body of clinical and experi-
mental evidence has challenged the classic paradigm of

undisturbed bone healing for the osseointegration of den-
tal implants (Adell et al., 1981; Albrektsson et al., 1981).
Numerous studies demonstrated the principal value of im-
mediate and early loading and consensus statements have
been published (Cochran et al., 2004). Numerous criteria
regarding implant design, bone quality and functional
conditions have been postulated for segregating cases
0.5
0.4 Primary bone to implant contact
Secondary bone to implant contact
Bone to implant contact
0.3
0.2
0.1
0.0
N= 4 4 3 3
4 weeks 6 months
Fig. 5 e Bone contact rates after 4 weeks and 6 months (failed implant
excluded). The boxplot represent the primary bone contact and new
bone formation/remodelling rates. (Heavy line: median, box covers 25e
75% percentiles, whiskers mark maximum and minimum values).
Fig. 6 e Fluorescence microphotograph after 4 weeks (50). Rather
diffuse incorporation of the fluorochrome administered at postoperative
day 7, predominantly around the bone adjacent to the drilling site.
Primary loading of palatal implants 25
suitable for early loading from those requiring unloaded
osseointegration. Besides poor bone quality (type IV),
short (length below 10 mm) and thin implants (diameter
below 4 mm) have been considered to jeopardize success
under prosthetic loading (Chiapasco et al., 1997; Tarnow
et al., 1997; Horiuchi et al., 2000). These recommenda-
tions, however, were mainly derived from gross clinical
experience rather than sound experimental evidence, leav-
ing the critical bone properties and the exact critical length
and diameter of immediately loaded implants as open
issues.
Although the loading conditions of palatal implants
clearly set them apart from prosthetic loading conditions,
there are multiple factors that might exclude early func-
tional loading for these, i.e. the reduced length and the
small diameter of these implants might not enable pri-
mary stability usually considered adequate for immediate
loading. A final insertion torque of 32e40 N cm, is pos-
tulated to correlate with sufficient primary stability (Ho-
riuchi et al., 2000; Malo et al., 2000), but cannot be
achieved with the small amount of bone available in
the midpalatal region. However, regarding the direction,
duration and dimensions of orthodontic forces, it has to
be questioned whether the strict limitations just men-
tioned should also be applied to implants used for ortho-
dontic anchorage. Hence the need for this animal
experiment.
It might be argued, that orthodontic loading conditions
are not fully reflected in this experiment which only ap-
plied constant ‘‘static’’ forces by means of coil springs.
However, it is the most prominent characteristic of Nie
Ti coil springs, that they exert quasi ‘‘static’’ traction
forces over a wide range of linear axial deformation.
Thus, the loading characteristics applied in this study
seemed adequate to imitate orthodontic anchorage.
The overall rather low bone-contact rates in this study
impressed, as values of about 75e80% have already
been described for implants with SLA-surfaces (Perrin
et al., 2002; Buser et al., 2004). However, Aldikaçti et
al. (2004) reported substantially lower rates (40%) in
maxillary SLA-implants under loading conditions with
orthodontic forces. Comparable rates (38%) could be
calculated for the present study, when the apical portion
of the implants, protruding towards the nasal cavity were
excluded from the morphometrical analysis (data not
shown).
Although in this study all implants were kept in place
and seem to support the principle of immediate loading
in orthodontic palatal implants. However, the histological
evaluation gave rise to doubts with respect to the safety of
osseointegration. The almost absent bone contact in one of
eight implants indicates, that the experimental protocol
approached the borderline of a reliable clinical procedure.
At least, the failure of osseointegration suggested that
clinical failure of the implant would follow soon.
The morphometrical analysis of bone to implant con-
tact suggested, that at 4 weeks after insertions, the initial
mechanical retention still provided a major contribution
to the implant stability in the four implants tested (about
50% of the overall bone to implant contact). New bone
formation had already been initiated, but the major pro-
portion of remodelling occurred later. When looking at
26 Journal of Cranio-Maxillofacial Surgery
Fig. 7 e a: Fluorescence microphotograph after 6 months (50). Both fluorochromes administered at the first (xylene orange) and second (calcein
green) postoperative months are incorporated as clearly defined bands. b: Fluorescence microphotograph after 6 months (100). Intense fluorochrome
apposition in the bony trabeculae.
the final 26% bone to implant contact rate in the 3 (out of
4) implants clinically and histologically classified as suc-
cessful after 6 months, it is intriguing to note, that there
was only a small difference from the values measured af-
ter 4 weeks (19%). Extrapolating the data, one might
conclude, that sufficient osseointegration as was required
for stability against orthodontic forces, already existed 4
weeks after surgery. This corresponds well to the find-
ings of the polychrome sequential labelling, where in-
tense mineral deposition in the bony trabecula around
the implant (indicating remodelling) was noted at 1 and
2 months after surgery. One further detail may be
of interest: the fluorochrome bands representing mineral-
ization at 1 month (red) and 2 months (green)
postoperatively were only scarcely seen in direct contact
to the implant surface. This suggests, that the genuine os-
seointegration process was almost complete at that time.
CONCLUSION
In this study, borderline reliability of osseointegration for
immediately loaded palatal implants but reasonable bone
formation until the fourth postoperative week was found
histologically. Thus it seems likely that sufficient second-
ary stability for early orthodontic loading can be ex-
pected after 4 weeks.
ACKNOWLEDGMENTS
This work was supported in part by a grant of the Institute Strau-
mann AG, CH-4437 Waldenburg, Switzerland to Martin Kunkel.
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Prof. Dr. Dr. M. KUNKEL
Department of Oral and Maxillofacial Surgery
University Hospital of Mainz
Augustusplatz 2 55101 Mainz
Tel.: 0049 6131 173191
Fax: 0049 6131 176602
E-mail: kunkel@mkg.klinik.uni-mainz.de
Paper received 24 March 2006
Accepted 5 July 2007