Int. J. Oral Maxillofac. Surg.

2008; 37: 741–747

doi:10.1016/j.ijom.2008.04.017, available online at http://www.sciencedirect.com

Research Paper
Oral Surgery

Dimensional ridge alterations D.

M.
K.
Rothamel1, F. Schwarz2,
Herten2, E. Engelhardt3,
Donath4, P. Kuehn2,
Becker2
following socket preservation J.
1
Department of Maxillofacial and Plastic
Surgery, University of Cologne, Cologne,
Germany; 2Department of Oral Surgery,

using a nanocrystalline Heinrich Heine University, Düsseldorf,

Germany; 3Animal Research Institute,
Heinrich Heine University, Düsseldorf,

hydroxyapatite paste. A Germany; 4Pathologist, Rödinghausen,

Germany

histomorphometrical study in
dogs§
D. Rothamel, F. Schwarz, M. Herten, E. Engelhardt, K. Donath, P. Kuehn, J. Becker:
Dimensional ridge alterations following socket preservation using a nanocrystalline
hydroxyapatite paste. A histomorphometrical study in dogs. Int. J. Oral Maxillofac.
Surg. 2008; 37: 741–747. # 2008 International Association of Oral and Maxillofacial
Surgeons. Published by Elsevier Ltd. All rights reserved.

Abstract. The aim of the study was to evaluate the histological response and
dimensional ridge alterations following application of a nanocrystalline
hydroxyapatite paste (NHA) into fresh extraction sockets in dogs. Immediately
following vertical tooth separation and extraction, NHA was inserted in the
extraction socket of the second molar in the lower jaws of 10 dogs. Untreated
extraction sites on the opposite side served as controls. Wounds were closed using
resorbable sutures after vertical flap elevation. After three and six months, 5 animals
were killed. Lingual and buccal bone height, alveolar wall and total bone width 1, 3
and 5 mm underneath the top of the crest were evaluated. Histological analysis
revealed a high variability of NHA resorption and osteoconductive properties with
different rates of material resorption. No statistically significant differences could
be observed between the corresponding aspects of test and control sites. Both groups
revealed higher alveolar wall resorption on the buccal than on the lingual side at
Keywords: animal study; ridge alterations;
both time periods. NHA does not seem to be useful for socket preservation
wound healing; extraction; implant therapy;
procedures since it failed to prevent dimensional ridge alterations while revealing socket preservation.
osseous integration but unpredictable material resorption. The role of non-resorbed
hydroxyapatite remnants for implant placement is unclear and requires further Accepted for publication 17 April 2008
investigation. Available online 12 June 2008

§
The study was funded by a grant from Heraeus Kulzer, Hanau, Germany.

0901-5027/080741 + 07 $30.00/0 # 2008 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
742 Rothamel et al.
Oral rehabilitation with dental implants
requires sufficient bone configuration in
both vertical and horizontal dimensions.
The preservation of extraction wounds
plays a central role in alveolar ridge main-
tenance after dental extraction. The phy-
siological atrophy that occurs during
dynamic bone regeneration of the extrac-
tion socket simplifies implant insertion
and improves predictability without the
need for additional augmentative therapy.
This reduces the duration of therapy,
improves the aesthetics and reduces stress
for the patient.
The physiological processes of wound
healing after tooth extraction may be
described in 5 steps: formation and
maturation of a blood coagulum (day 1);
organization of the coagulum by capil-
laries (4–5 days); formation of a tempor-
ary matrix (14–16 days); osteoblastic
reorganization of the temporary matrix
and complete epithelial closure of the
alveolus (until 6 weeks); bone modelling/
remodelling (5–10 weeks)1,7.
The morphological changes in the
alveolar process in the apical–coronal
and buccal–lingual directions after extrac-
tion have been determined in many
pre-clinical and clinical studies3,18,25.
Concerning dimensional changes of the
bone after dental extraction, a loss of
vertical and horizontal bone volume was
observed. Especially for the maxilla,
resorptional changes in the buccal bone
wall of the alveolus have been described,
resulting in an oral shift of the alveolar
process3,23. Atrophy seems to be particu-
larly distinct during the first 3 months after
dental extraction25. Regular resorption of
the bone matrix depends on the position of
the extracted tooth25, the size of the defect
and the composition of the surrounding
bone5,28. Negative parameters for wound
healing include severe periodontitis of
the extracted tooth, uncareful extraction
methods and wound infection13,22.
Increased age may initially have an inhi-
bitory effect on the development of provi-
sional bone matrix. This influence was not
evident after a healing period of 40 days2.
In a study comparing hydroxyapatite in
solid and particulate form, neither pre-
vented bone resorption after tooth extrac-
tion, although particles were better at
physically maintaining ridge height and
width6.
The insertion of bone substitute mate-
rial into the fresh extraction socket may
have a positive effect on wound healing
and avoid atrophy of the alveolar bone.
Any applied material alters the normal
sequence of healing. Depending on the
material properties and the size and shape
of the inserted particles, resorption, oss-
eous integration/organization and soft tis-
sue encapsulation can be observed.
Biodegradation is directly influenced by
the type of material crystallisation20.
Depending on the material properties
and on the size of the inserted particles,
biphasic calcium phosphate particles
affected cellular-degradation activity but
not bone-filling ability11.
Preliminary experimental studies have
shown that nanosized ceramics may repre-
sent a promising class of bone graft sub-
stitutes owing to their improved
osseointegrative properties9,30. A ready-
to-use paste in a syringe, available under
the name OstimTM (Heraeus Kulzer,
Hanau, Germany) containing nanoscopic
apatite particles (35%) in aqueous disper-
sion, has recently been recommended for
augmentation procedures in osseous
defects9. Experimental animal studies
have suggested osseous integration and
complete resorption of the material within
12 weeks9,29. Owing to its specific physi-
cochemical properties, nanocrystalline
hydroxyapatite paste (NHA) is intended
to be used with or without the additional
application of a barrier membrane. Preli-
minary clinical results have shown that
the application of NHA resulted in a pre-
dictable resolution of peri-implantitis
defects26.
These data indicate that NHA might
also possess some physicochemical prop-
erties promoting wound healing in extrac-
tion sockets. Hypothetically, immediately
after application the nanoparticles in the
paste build a three-dimensional superficial
protein coverage. This could reduce the
inflammatory response, support the fast
osseous organization of the defect and
subsequently avoid the naturally occurring
resorption of the alveolar bone after tooth
extraction. While other small hydroxya-
patite particles are resorbed very slowly by
multinucleated (osteoclast-like) giant
cells15,27,32, nanosized soluble ceramics
are considered to be directly incorporated
by resorptive cells. The aim of the present
study was to evaluate the histological
response and dimensional ridge alterations
following application of NHA to the
extraction sockets of dogs.
Materials and Methods
The study protocol was approved by the
local Ethics Committee for Animal
Research. Ten 18-month-old foxhounds
(approximate weight 32 kg) were used
in the study. All animals exhibited a fully
erupted, healthy, permanent dentition.
After tooth extraction, the dogs were fed
once a day with a soft-food diet and water.
Animal selection, management, and the
surgery protocol were approved by the
Animal Care and Use Committee of Dues-
seldorf, Germany. The experimental seg-
ment of the study started after an
adaptation period of 4 weeks.
Study design
Study design was based on a study proto-
col published by Block and Kent in 19866.
In 10 adult dogs, the second molar teeth of
the lower jaws were extracted carefully
and the extraction sockets were either
filled with NHA or remained unfilled as
a control side, according to a randomized
split mouth design. After three and six
months, 5 animals were killed and speci-
mens were prepared for histological and
histomorphometrical analysis (n = 5).
Surgical procedure
After intramuscular sedation with
0.17 mg/kg acepromazine (Vetranquil
1%, Ceva Tiergesundheit, Düsseldorf,
Germany), anaesthesia was started using
21.5 mg/kg thiopental sodium (Trapanal
2.5%, Altana GmbH, Konstanz, Ger-
many). For surgical procedures inhalation
anaesthesia was performed using oxygen,
nitrous oxide and isoflurane. To maintain
hydration, animals received a constant rate
infusion of lactated Ringer’s solution
while being anaesthetized. Intraoperative
analgesia was provided by intravenous
injection of 0.4 mg/kg piritramide (Dipi-
dolor1, Janssen-Cilag GmbH, Neuss,
Germany) and 4.5 mg/kg carprofene
(Rimadyl1, Pfitzer Pharma GmbH, Karls-
ruhe, Germany). For postoperative treat-
ment, piritramide and carprofene were
applied subcutaneously for three days at
the dose described. Additionally, clinda-
mycin (11.0 mg/kg body weight, Cle-
robe1, Pharmacia Tiergesundheit,
Erlangen, Germany) was administered
prophylactically intra- and postopera-
tively for 3 days.
The second molar teeth (M2) of the
lower jaws were carefully removed after
vertical tooth separation. The extraction
socket of one side, selected at random, was
filled completely with NHA (Ostim1,
Heraeus Kulzer, Hanau, Germany), while
the control side remained unfilled.
Wounds were closed after vertical flap
elevation using resorbable mattress
sutures (Resorba, Nürnberg, Germany).
After a healing period of 3 and 6 months,
five animals each were killed (overdose of
 Dimensional ridge alterations 743

wall to the most apical point of the jaw,

Fig. 1. a Histomorphometrical parameters evaluated for vertical parameters: buccal bone height
(BBH) and lingual bone height (LBH). b Histomorphometrical parameters evaluated for
horizontal parameters: lingual and buccal alveolar wall width 1, 3 and 5 mm infracrestally
(A, B, C); lingual and buccal total bone width (A0 , B0 , C0 ) measured perpendicular to the long
axis of the extraction socket.
sodium pentobarbital, 200 mg/kg i.v.)
after intravenous injection of 50 000 i.E.
heparin. After preparation and catheteri-
zation of the carotid arteries, decapitation
was performed and the head of the animal
was intra-arterially fixed with 1000 ml of
4% buffered formalin solution. Following
this primary fixation procedure, the jaws
were dissected to obtain the blocks con-
taining the experimental specimens or
corresponding control sites. The speci-
mens were fixed in 4% neutral buffered
formalin solution for 7 days. The samples
were then dehydrated using ascending
grades of alcohol, and infiltrated and
embedded in special glycol methacrylate
resin (Technovit 7200VLC, Heraeus Kul-
zer, Wehrheim, Germany) for nondecalci-
fied sectioning. Each specimen was cut in
the bucco-oral direction along the axis of
the extraction socket using a diamond
band saw (Exakt, Apparatebau, Norder-
stedt, Germany), resulting in three sec-
tions of approximately 200 mm
thickness10. All specimens were glued
with acrylic cement (Technovit 7210
VLC, Heraeus Kulzer, Wehrheim, Ger-
many) to opaque plastic and ground to a
final thickness of 40 mm. All sections were
stained with toluidine blue after superficial
etching and decalcification with 20%
hydrogen peroxide and 10% formic acid.
images were obtained using a light micro-
scope (BX50, Olympus, Hamburg, Ger-
many) at a magnification of 12.5 and
40, associated with a camera (SIS Color
View3, Soft imaging System GmbH,
Münster, Germany). Digital images were
evaluated using a software program (SIS
analySIS Auto Software 3.2, Soft imaging
System GmbH, Münster, Germany). The
following lateral aspects of the extraction
sockets were evaluated: lingual and buccal
total bone height (LBH, BBH: measured
from the top of the buccal and oral alveolar
Fig. 1a); lingual and buccal alveolar wall
bone width (A, B, C) and total bone width
(A0 , B0 , C0 ) (measured perpendicular to the
long axis of the extraction socket 1, 3 and
5 mm underneath the top of the respective
bone crest, Fig. 1b). For statistical analy-
sis, the difference between the buccal and
oral top of the alveolar crest (LBH–BBH)
was calculated.
A software package (SPSS 12.0, SPSS
Inc., Chicago, IL, USA) was used for
statistical analysis. Depending on the
cross arch design, Wilcoxon tests were
used for inductive statistics between the
test and control sites of each animal. Dif-
ferences were considered statistically sig-
nificant at a level of P < 0.05.
Results
All extraction sockets healed unevent-
fully. No infections or wound dehiscence
were observed during the study period.
Three-month specimens
For NHA specimens, the histological
appearance and bone substitute resorption
varied. Two extraction sockets were
almost completely filled with remnants
of the bone substitute material (Fig. 2a);
three specimens displayed a medium or
high grade of NHA resorption. For minor-
resorbed specimens, the crestal part of the
alveolus was separated by slight newly

Histological and histomorphometric
analysis
Histomorphometrical analyses and micro-
scopic observations were performed by
one experienced investigator blinded
to the specific experimental conditions.
For histomorphometrical measurements,
Fig. 2. a For this low-resorbed 3-month NHA specimen, the bone defect is almost completely
filled by the remnants of the bone substitute material. In the apical part of the alveolus, a
separation of the graft by a compact bone layer and soft-tissue gap can be observed (original
magnification 12.5). b Higher magnification of the crestal part of the alveolus. Augmented
areas are separated by newly formed bone bridges and covered by soft tissue (original
magnification 40). c The non-resorbed hydroxyapatite particles are demonstrating a three-
coloured surface with the presence of numerous multinuclear giant cells and macrophages
(original magnification 600).
744 Rothamel et al.

non-resorbed NHA particles seemed to be

smaller than the particles observed for the
3-month specimens and displayed more
horizontal bony separation. Most of the
remnants displayed small bone coverage,
but some single NHA particles were still
encased by soft tissue and surrounded by
multinucleated giant cells and macro-
phages. For the control group, no differ-
ence was observed between the old and the
newly formed bone tissue. The defects
were completely ossified and the cancel-
lous bone was covered with a round,
compact bone layer on the crest and nor-
mal gingival tissue (Fig. 6a–c).

Histomorphometrical analysis
Means and standard deviations of the
Fig. 3. a Histological section of 3-month control site. The soft tissue is covering the defect, but parameters measured are displayed in
no signs of closure of the alveolar crest with compact bone could be observed. The cancellous Tables 1–3. No aspect revealed statisti-
areas are still open to the soft tissue (original magnification 12.5). b Higher magnification of cally significant differences between the
(a). Young, minor calcified bony tissue is filling the defect. No gaps between the alveolar wall
test and control sites of each animal
and the former extraction socket can be observed. Young, minor calcified bone is forming an
interconnective system with the alveolar wall (original magnification 40). c Higher magni- (P > 0.05, Wilcoxon test). The LBH
fication of (a). Howshiṕs lacunae can be found on the outline of the alveolar crest, representing was significantly higher than the BBH
ongoing bone resorption (original magnification 200). for both time periods and groups
(P < 0.05, Wilcoxon test, respectively).

formed horizontal bone bridges separating areas. In line with the three-month results,
Discussion
the NHA areas. The apical portion of the extraction sockets showed various
NHA-augmented area was more amor- amounts of non-resorbed NHA particles. Few histological studies on the bone sub-
phous and revealed a gap between the Two specimens displayed high resorption stitute material used in the study can be
alveolar wall and the bone substitute. A rates and subsequently small remnants of found in the literature. HUBER et al.14 eval-
compact bone layer with no penetrating NHA (Fig. 4a–c); two extraction sockets uated bone regeneration after insertion
blood vessels was observed on the surface revealed very low graft resorption with of NHA in cancellous bone in a human
of the previous alveolar wall (Fig. 2b). large NHA areas that were partially sepa- traumatological study. The human bone
Under higher magnification, the NHA par- rated from the surrounding alveolar bone biopsies taken during the removal of
ticles displayed differently intensive by a gap up to 0.5 mm (Fig. 5a–c). The osteosynthetic plates showed good regen-
coloured areas. Approaching the surface,
the blue amorphous NHA core was
replaced by a small, dark-blue layer. For
osseointegrated particles the dark surface
was encased by a non-coloured area with
signs of crystallization underneath the first
small bone layer, the non-osseointegrated
particles were enclosed by soft tissue and
surrounded by macrophages and multinu-
cleated giant cells (Fig. 2c).
For the control group, the extraction
sockets were filled with low-calcified can-
cellous bone. The reduced calcification of
this fresh bone was marked by the more
intensive staining of toluidine blue. The
spongiosa areas of the alveolar crest were
opened to the soft tissue, although remodel-
ling of the alveolar crest with compact bone
seemed to be continuing and a high number
of Howship’s lacunae could be observed on
the alveolar surface (Fig. 3a–c).
Fig. 4. a Histological section of a major-resorbed 6-month NHA site. Small particles of the bone
Six-month specimens substitute are still present in the crestal part of the former alveolus (original magnification
12.5). b Higher magnification of (a). Crestal particles are surrounded by new bone tissue
Six-month specimens of NHA revealed (original magnification 40). c Higher magnification of (a). Even in the apical part of the
compact bone layers covering the defect extraction socket small remnants of NHA can be found (original magnification 200).
 Dimensional ridge alterations 745

(Fig. 2c). The variability in the coloration

of the particles could be based on their
various calcification rates. The lower the
calcification rate the higher the intensity of
the staining of the mineralized tissues. The
more intensive staining on the surface of
the particles could be the result of resorp-
tion processes initiated by the surrounding
tissue.10 The completely decalcified line
on the osseointegrated surfaces provides
for new bone formation, as displayed in
the presence of new crystallization nuclei
observed at the transition layer with the
adjacent bone. These histological obser-
vations emphasize the necessity for com-
plete NHA resorption before rebuilding
new hard tissue.
Non-resorbed NHA remnants were
observed in a study of human acetabular
Fig. 5. a Histological section of a minor-resorbed 6-month NHA site. Remnants of the bone bone impaction grafting.9 In that study,
substitute are still present and surrounded by a gap of up to 0.5 mm (original magnification NHA was a 10% addition to mixtures
12.5). b Higher magnification of (a). Complete hard tissue healing on the alveolar crest of morselized cancellous bone (MCB)
(original magnification 40). c Higher magnification of (a). Osseointegrated remnants of NHA and/or tricalcium phosphate–hydroxyapa-
are surrounded by small layers of vital, newly formed bone (original magnification 200x). tite (TCP-HA) granula as a reductor for
cement penetration during acetabular
reconstruction. In the histological sec-
tions, most of the NHA was osseous-inte-
grated with MCB or TCP-HA granules
after 8 weeks. In line with the present
authors’ results, specifically stained sec-
tions revealed that some NHA remnants
had actively been resorbed by multinu-
cleated giant cells and macrophages.9
The previous results of an experimental
study in pigs revealed complete resorption
of the material after 12 weeks.29 In this
study, critical size calvarial defects were
prepared and filled with NHA, autologous
bone (AB) or NHA/AB (25%). The micro-
radiographic and histological evaluation
indicated mineralization rates in the two
bone substitute groups that were not sig-
nificantly lower than those found for the
Fig. 6. a Histological section of 6-month control site (original magnification 12.5). The bone AB group29. The contrast to the present
tissue displays a uniform mineralization. No indicators of the former extraction socket are
visible. b Higher magnification of (a). Complete hard and soft tissue healing with formation of a
study may be explained because the inser-
compact bone layer on the alveolar crest. No signs of Howship’s lacunae can be observed tion of the biomaterial was limited to acute
(original magnification 40). c Higher magnification of (a). Cancellous bone is filling the space defects with different localization than the
underneath the alveolar crest (original magnification 40). alveolar bone. The influence of the experi-
mental model (human or different kinds of
eration in the allocated areas with regular stitute were detected as amorphous mate- animals) also has to be considered. The
bone turnover. In line with the present rial in adjacent tissue. These particles were slower resorption rate could be a result of
results, severe inflammatory reactions, also found in the present study, mostly the different shape of the replaced area. In
osteofibrosis or osteonecrosis caused by enclosed by bone tissue or in the case of the course of most other studies the appli-
the bone substitute material were not soft-tissue encapsulation surrounded by cation of NHA was limited to acute gaps
observed.14 Small parts of the bone sub- some resorptive cells on the surface between bone walls, whereas after a dental

Table 1. Means and standard deviations of buccal (BBH) and lingual bone height (LBH) and bone height difference (BBH-LBH)
3 months 6 months
P P
NHA mean (SD) Control mean (SD) NHA mean (SD) Control mean (SD)
BBH 23.67 (0.63) 22.98 (0.73) 0.465 23.47 (2.19) 23.93 (0.88) 0.465
LBH 24.21 (0.19) 23.83 (0.63) 1.000 24.61 (2.21) 25.00 (0.93) 0.273
BBH-LBH 0.54 (0.62) 0.85 (0.17) 0.715 1.14 (0.54) 1.07 (0.80) 0.465
NHA, nanocrystalline hydroxyapatite paste.
746 Rothamel et al.

Table 2. Means and standard deviations of lingual and buccal alveolar wall thickness on different levels: 1 mm (A), 3 mm (B) and 5 mm (C)
3 months 6 months
P P
NHA mean (SD) Control mean (SD) NHA mean (SD) Control mean (SD)
Level A buccal 2.98 (0.30) 3.06 (0.29) 0.465 1.98 (0.56) 2.16 (0.51) 0.273
Level B buccal 3.38 (0.32) 3.54 (0.28) 0.273 2.09 (0.45) 2.31 (0.39) 1.000
Level C buccal 3.82 (0.43) 3.87 (0.28) 0.068 2.27 (0.30) 2.54 (0.07) 0.715
Level A lingual 3.25 (0.29) 3.16 (0.40) 0.715 1.65 (0.35) 1.69 (0.34) 0.273
Level B lingual 3.73 (0.27) 3.50 (0.29) 0.144 2.06 (0.17) 2.17 (0.25) 0.465
Level C lingual 3.91 (0.31) 3.61 (0.19) 0.465 2.53 (0.15) 2.73 (0.39) 0.465
NHA, nanocrystalline hydroxyapatite paste.

Table 3. Means and standard deviations of lingual and buccal total bone thickness on different levels: 1 mm (A0 ), 3 mm (B0 ) and 5 mm (C0 )
3 months 6 months
P P
NHA mean (SD) Control mean (SD) NHA mean (SD) Control mean (SD)
Level A0 buccal 1.80 (0.26) 1.49 (0.32) 0.715 3.22 (0.85) 3.46 (0.38) 1.000
Level B0 buccal 1.79 (0.13) 1.78 (0.53) 0.465 3.72 (1.23) 3.89 (0.50) 0.465
Level Ć buccal 2.16 (0.33) 2.01(0.23) 0.715 4.09 (1.58) 4.22 (0.55) 0.715
Level A0 lingual 1.75 (0.66) 1.40 (0.42) 1.000 3.66 (0.61) 3.75 (0.50) 0.715
Level B0 lingual 1.82 (0.45) 1.70 (0.42) 1.000 4.17 (0.93) 4.27 (0.56) 0.273
Level C0 lingual 2.07 (0.48) 1.91 (0.62) 0.715 4.30 (1.11) 4.50 (0.52) 0.273
NHA, nanocrystalline hydroxyapatite paste.

extraction the shape of the defect corre-
sponds to the root configuration and espe-
cially in the crestal region it is therefore
much thicker. The depth of the primary
invasion of blood components into the
hydroxyapatite suspension could play a
major role in the subsequent osseous orga-
nization of the graft material. Several
studies suggest that for granular hydro-
xyapatite pore sizes smaller than 100 mm
inhibit blood vessel in growth and bone
formation12,16. Concerning the gaps sur-
rounding some graft areas, the compact
bone line on the boundary of the former
alveolar wall can be interpreted as a
demarcation of the graft, particular since
no penetrating blood vessels could be
observed (Fig. 4c). Shrinking of the bone
substitute during primary wound organi-
zation or an influence from the periodontal
ligament cells should also be considered.
CARDAROPOLI et al.8 investigated the role of
the periodontal ligament in extraction
socket healing. No difference was found
between socket healing after periodontal
ligament removal and control sites within
3 months of healing period. These findings
suggest that the role of the periodontal
ligament is not essential for the healing
procedure.
In contrast to other studies, the applica-
tion of NHA did not lead to a reduction of
the naturally occurring reduction of the
absolute bone height. In other animal stu-
dies, the vertical atrophy of the alveolar
ridge was reduced compared with untreated
alveolus after infracrestal implantation of
preformed root-like hydroxy tapers24, par-
ticulated hydroxyapatite17 and ß-trical-
ciumphosphate root tapers. Although
resorption of the ß-tricalciumphosphate
granula was histologically found within a
period of 60 weeks, it seemed that the
regeneration of the extraction alveolus
was slowed down compared with the
untreated control group21. The deceleration
observed is in line with the present findings,
because in this study complete hard tissue
healing was observed after 6 months for the
control but not for the NHA group. By using
a membrane either with31 or without the
support of a filling material18,19 it was
possible to stop the dimensional changes
of the alveolar ridge after dental extraction.
In a clinical trial, LEKOVIC et al.19 showed
that after 6 months, fresh extraction sockets
covered with polytetrafluoroethylene
(ePTFE) membranes are subject to signifi-
cantly smaller dimensional changes of the
alveolar ridge compared with untreated
control sockets. Comparable results were
obtained using polylactide/polyglycolide
membranes although early exposure of
the membrane led to significant deteriora-
tion of the clinical results18.
The significantly higher resorption on
the buccal side is in line with an extraction
study by ARAUJO et al.3 Over a period of 8
weeks after tooth extraction, the vertical
distance between the buccal and lingual
intersections increased with time after
initial superposition of the buccal aspect
after one week. In another animal study,
not even the instant insertion of screw-
shaped titanium implants into fresh extrac-
tion sockets could compensate for the
resorptional changes of the buccal com-
pacta. Within 3 months a distinct vertical
loss of bone of about 2 mm occurred in
this area4.
Within the limits of the present study it
was concluded that NHA is not useful for
socket preservation procedures since it
failed to prevent dimensional ridge altera-
tions while revealing osseous integration
but unpredictable material resorption. The
role of the non-resorbed hydroxyapatite
remnants for implant placement is still
unclear and requires further investigation.
Conflict of Interests
The authors declare that they have no
conflict of interests.
Acknowledgements. We gratefully thank
Mrs Brigitte Hartig for her excellent tech-
nical expertise in specimen preparation.
References
1. Amler MH. The time sequence of tissue
regeneration in human extraction
wounds. Oral Surg Oral Med Oral Pathol
1969: 27: 309–318.
2. Amler MH. Age factor in human alveolar
bone repair. J Oral Implantol 1993: 19:
138–142.
3. Araujo MG, Lindhe J. Dimensional
ridge alterations following tooth extrac-
tion. An experimental study in the dog. J
Clin Periodontol 2005: 32: 212–218.
4. Araujo MG, Sukekava F, Wennstrom
JL, Lindhe J. Ridge alterations following
implant placement in fresh extraction
sockets: An experimental study in the
dog. J Clin Periodontol 2005: 32: 645–
652.
5. Atwood DA. Some clinical factors
related to rate of resorption of residual

ridges. 1962. J Prosthet Dent 2001: 86:
119–125.
6. Block MS, Kent JN. A comparison of
particulate and solid root forms of hydro-
xyapatite in dog extraction sites. J Oral
Maxillofac Surg 1986: 44: 89–93.
7. Boyne PJ. Osseous repair of the postex-
traction alveolus in man. Oral Surg Oral
Med Oral Pathol 1966: 21: 805–813.
8. Cardaropoli G, Araujo M, Hayaci-
bara R, Sukekava F, Lindhe J. Healing
of extraction sockets and surgically pro-
duced - augmented and non-augmented -
defects in the alveolar ridge. An experi-
mental study in the dog. J Clin Period-
ontol 2005: 32: 435–440.
9. Chris Arts JJ, Verdonschot N,
Schreurs BW, Buma P. The use of a
bioresorbable nano-crystalline hydroxya-
patite paste in acetabular bone impaction
grafting. Biomaterials 2006: 27: 1110–
1118.
10. Donath K. The diagnostic value of the
new method for the study of undecalcified
bones and teeth with attached soft tissue
(sage-schliff (sawing and grinding) tech-
nique). Pathol Res Pract 1985: 179: 631–
633.
11. Gauthier O, Bouler JM, Weiss P,
Bosco J, Aguado E, Daculsi G.
Short-term effects of mineral particle
sizes on cellular degradation activity after
implantation of injectable calcium phos-
phate biomaterials and the consequences
for bone substitution. Bone 1999: 25:
71S–74S.
12. Holmes RE, Bucholz RW, Mooney V.
Porous hydroxyapatite as a bone-graft
substitute in metaphyseal defects. A his-
tometric study. J Bone Joint Surg Am
1986: 68: 904–911.
13. Houston JP, McCollum J, Pietz D,
Schneck D. Alveolar osteitis: A review
of its etiology, prevention, and treatment
modalities. Gen Dent 2002: 50: 457–463
quiz 464-455.
14. Huber FX, Belyaev O, Hillmeier J,
Kock HJ, Huber C, Meeder PJ, Berger
I. First histological observations on the
incorporation of a novel nanocrystalline
hydroxyapatite paste ostim in human can-
cellous bone. BMC Musculoskelet Disord
2006: 7: 50.
15. Kawaguchi H, Ogawa T, Shirakawa
M, Okamoto H, Akisaka T. Ultrastruc-
tural and ultracytochemical characteris-
tics of multinucleated cells after
hydroxyapatite implantation into rat per-
iodontal tissue. J Periodontal Res 1992:
27: 48–54.
16. Klawitter JJ, Hulbert SF. Application
of porous ceramics for attachment of load
bearing internal orthopedic applications. J
Biomed Mater Res 1971: 10: 161–229.
17. Kwon HJ, el Deeb M, Morstad T,
Waite D. Alveolar ridge maintenance
with hydroxyapatite ceramic cones in
humans. J Oral Maxillofac Surg 1986:
44: 503–508.
18. Lekovic V, Camargo PM, Klokkevold
PR, Weinlaender M, Kenney EB,
Dimitrijevic B, Nedic M. Preservation
of alveolar bone in extraction sockets
using bioabsorbable membranes. J Peri-
odontol 1998: 69: 1044–1049.
19. Lekovic V, Kenney EB, Weinlaender
M, Han T, Klokkevold P, Nedic M,
Orsini M. A bone regenerative approach
to alveolar ridge maintenance following
tooth extraction. Report of 10 cases. J
Periodontol 1997: 68: 563–570.
20. Lu J, Descamps M, Dejou J, Koubi G,
Hardouin P, Lemaitre J, Proust JP.
The biodegradation mechanism of cal-
cium phosphate biomaterials in bone. J
Biomed Mater Res 2002: 63: 408–412.
21. Nair PN, Luder HU, Maspero FA,
Fischer JH, Schug J. Biocompatibility
of {beta}-tricalcium phosphate root repli-
cas in porcine tooth extraction sockets - a
correlative histological, ultrastructural,
and x-ray microanalytical pilot study. J
Biomater Appl 2006.
22. Nicopoulou-Karayianni K, Bragger
U, Lang NP. Patterns of periodontal
destruction associated with incomplete
root fractures. Dentomaxillofac Radiol
1997: 26: 321–326.
23. Pietrokovski J, Massler M. Alveolar
ridge resorption following tooth extrac-
tion. J Prosthet Dent 1967: 17: 21–27.
24. Sattayasanskul W, Brook IM, Lamb
DJ. Dense hydroxyapatite root replica
implantation: Measurement of mandibu-
lar ridge preservation. Int J Oral Maxil-
lofac Implants 1988: 3: 203–207.
25. Schropp L, Wenzel A, Kostopoulos
L, Karring T. Bone healing and soft
tissue contour changes following single-
tooth extraction: A clinical and radio-
Dimensional ridge alterations 747
graphic 12-month prospective study. Int
J Periodontics Restorative Dent 2003: 23:
313–323.
26. Schwarz F, Bieling K, Latz T,
Nuesry E, Becker J. Healing of intrab-
ony peri-implantitis defects following
application of a nanocrystalline hydro-
xyapatite (ostim) or a bovine-derived
xenograft (bio-oss) in combination with
a collagen membrane (bio-gide). A case
series. J Clin Periodontol 2006: 33: 491–
499.
27. Takeshita N, Akagi T, Yamasaki M,
Ozeki T, Nojima T, Hiramatsu Y,
Nagai N. Osteoclastic features of multi-
nucleated giant cells responding to syn-
thetic hydroxyapatite implanted in rat jaw
bone. J Electron Microsc (Tokyo) 1992:
41: 141–146.
28. Tallgren A. The continuing reduction
of the residual alveolar ridges in complete
denture wearers: A mixed-longitudinal
study covering 25 years. 1972. J Prosthet
Dent 2003: 89: 427–435.
29. Thorwarth M, Schultze-Mosgau S,
Kessler P, Wiltfang J, Schlegel KA.
Bone regeneration in osseous defects
using a resorbable nanoparticular hydro-
xyapatite. J Oral Maxillofac Surg 2005:
63: 1626–1633.
30. Webster TJ, Ergun C, Doremus RH,
Siegel RW, Bizios R. Enhanced func-
tions of osteoblasts on nanophase cera-
mics. Biomaterials 2000: 21: 1803–
1810.
31. Wiesen M, Kitzis R. Preservation of the
alveolar ridge at implant sites. Period-
ontal Clin Investig 1998: 20: 17–20.
32. Yamada S, Nakamura T, Kokubo T,
Oka M, Yamamuro T. Osteoclastic
resorption of apatite formed on apatite-
and wollastonite-containing glass-cera-
mic by a simulated body fluid. J Biomed
Mater Res 1994: 28: 1357–1363.
Address
Daniel Rothamel
Department of Maxillofacial and
Plastic Surgery
University of Cologne
D - 50937 Cologne
Germany
Tel.: +49 221 478 7209
Fax: +49 221 478 7360.
E-mail: daniel.rothamel@uk-koeln.de