histomorphometric assessment in human cadavers of the peri-implant bone density in maxillary...
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Histomorphometric assessment inhuman cadavers of the peri-implantbone density in maxillary tuberosityfollowing implant placement usingosteotome and conventional techniques
Juan BlancoJuan SuarezSilvia NovioGabriel VillaverdeIsabel RamosLuis Alberto G. Segade
Authors’ affiliations:Juan Blanco, Gabriel Villaverde, Isabel Ramos,Department of Stomatology, Faculty of Medicineand Dentistry, University of Santiago deCompostela, Santiago, SpainJuan Suarez, Silvia Novio, Luis Alberto G. Segade,Department of Morphological Sciences, Faculty ofMedicine and Dentistry, University of Santiago deCompostela, Santiago, Spain.
Correspondence to:Dr Juan BlancoDepartment of StomatologyFaculty of Medicine and DentistryUniversity of Santiago de CompostelaEntrerrıos s/n.E-15705 Santiago de CompostelaSpainTel.: þ 34 981 571 826Fax: þ 34 981 571 620e-mail: [email protected]
Key words: bone quality, dental implant, implant stability, maxillary tuberosity, osteotome
Abstract
Objective: To evaluate and compare peri-implant bone condensation in the maxillary
tuberosity of human cadavers following the osteotome and standard drilling techniques,
and to determine whether peri-implant bone condensation following the osteotome
technique is localized or homogeneous.
Material and methods: Twenty-four cylinder-threaded titanium implants (12 on each side)
were placed in the left (standard technique) and right (osteotome technique with tapered
osteotomes for bone condensation, Straumanns
) maxillary tuberosities of 12 edentulous
posterior maxillae of deceased people who had bequeathed their bodies to the University
of Santiago de Compostela for medical-scientific research. After surgery, the implants were
removed with the surrounding bone, prepared using sawing and grinding technique and
examined histomorphometrically. The bone density (bone area/analyzed area) of the entire,
periapical (fifth apical) and pericylinder peri-implant areas was calculated, statistically
analyzed and compared with the bone density of the host cancellous maxillary bone.
Results: The bone density of the entire peri-implant area was statistically found to be
greater with the osteotome technique (39.38 � 9.67) than with conventional drilling
technique (31.06 � 5.9). This difference was greatest for the periapical zone (53.32 � 12.26
vs. 34.18 � 6.34). Nonetheless, in the pericylinder area no significant difference was found
between the two techniques (32.30 � 8.74 vs. 30.34 � 7.2).
Conclusion: Peri-implant bone condensation following the osteotome technique is not
homogeneously observed through the entire peri-implant area. A greater bone density was
achieved only in the fifth apical peri-implant area.
Currently, oral rehabilitation with im-
plant-supported prosthesis is considered
the therapeutic procedure of choice for
partially or completely edentulous pa-
tients. The success of this treatment is
mainly associated with the primary stabi-
lity of the dental implant, this being only
one of the fundamental criteria for ensuring
osseointegration (Albrektsson et al. 1981).
Initial stability depends on the macro and
microscopic design of the implant, the
surgical technique and primarily on the
quality of the host bone (Meredith 1998).
Poor quality bone (types 3 and 4) is often
found in the posterior maxilla (Lekholm &
Zarb 1985; Ulm et al. 1999; Ulm & Tepper
2004), precisely the area where the largest
numbers of dental implant failures have
been described in the literature (Jaffin &
Berman 1991; Balshi et al. 1995, 1999;
Jemt & Lekholm 1995). Titanium im-
plants with rough surface (Roccuzzo &
Wilson 2002; Bergkvist et al. 2004; Balshi
et al. 2005) and modified surgical techni-
Date:Accepted 15 July 2007
To cite this article:Blanco J, Suarez J, Novio S, Villaverde G, Ramos I,Segade LAG. Histomorphometric assessment in humancadavers of the peri-implant bone density in maxillarytuberosity following implant placement using osteotomeand conventional techniques.Clin. Oral Impl. Res. 19, 2008; 505–510doi: 10.1111/j.1600-0501.2007.01505.x
c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard 505
ques (Bahat 1992, 1993, 2000; Venturelli
1996; Fernandez & Fernandez 1997) have
permitted the placement of implants in the
posterior maxilla with a success rate simi-
lar to other oral regions with good quality
bone. One of the surgical alternatives to the
conventional drilling technique is the os-
teotome technique, which was initially
introduced to increase the primary stability
of dental implants in the posterior maxilla
(Summers 1994a, 1994b, 1994c, 1995).
When reviewing the clinical literature of
oral implants, it was found that the osteo-
tome technique was generally carried out
in combination with sinus floor elevation
(Coatoam & Krieger 1997; Horowitz 1997;
Bruschi et al. 1998; Komarnyckyj &
London 1998; Zitzmann & Scharer 1998;
Fugazzotto 2002; Rodoni et al. 2005).
The greater implant success rate of the
osteotome technique in the posterior
maxilla without additional sinus floor
elevation (Fernandez & Fernandez 1997;
Komarnyckyj & London 1998) has been
attributed to, among other factors, the peri-
implant trabecular condensation produced
by the osteotomes on the cancellous max-
illary bone. Nocini et al. (2000) have re-
ported the compression of peri-implant
trabecular bone with the osteotome techni-
que, i.e., the ‘corticalization’ of the implant-
future socket. Nevertheless, to our knowl-
edge, no histomorphometric study in the
human posterior maxilla has been performed
to demonstrate a significant increase in
peri-implant bone density in comparison
with the surrounding cancellous bone as a
result of the osteotome technique. Like-
wise, we are unaware of statistical studies
that have evaluated peri-implant bone den-
sity following the osteotome technique as
compared with the conventional drilling
technique. Hence, the aim of this study
was twofold: (a) to assess peri-implant bone
condensation in the maxillary tuberosity of
human cadavers following the osteotome
technique and the conventional drilling
techniques; (b) to determine whether
peri-implant bone condensation following
the osteotome technique is localized or
homogeneous.
Material and methods
Edentulous posterior maxillae were ob-
tained from 12 cadavers (10 males and
two females). The age of the deceased
ranged from 60 to 93 years. All subjects
had bequeathed their bodies to the Depart-
ment of Morphological Sciences of the
University of Santiago de Compostela for
medical-scientific research and training
purposes. Before implant placement, radio-
graphs were taken to ensure that both
posterior maxillae exhibited a similar tra-
becular bone pattern (Fig. 1a). Twenty-four
cylinder-threaded titanium implants
(Straumanns
, Waldenburg, Switzerland),
4.1 mm in diameter and 10 mm in length,
(12 on each side) were placed in the left
(standard technique) and right (osteotome
technique) tuberosities of the maxillae.
For the conventional technique, the im-
plant sites were sequentially enlarged to
3.5 mm in diameter with pilot and twist
drills according to the manufacturer’s pro-
tocol (Straumanns
). In the right maxillary
tuberosity, the implant sites were prepared
by a pilot drill, followed by twist drilling
of the cortical bone and finally prepar-
ing the cancellous maxillary bone by
tapered osteotomes of increasing diameter
(osteotome kit for bone condensation,
Straumanns
). Following implant place-
ment, radiographs were taken to ensure
that the implants had been correctly posi-
tioned (Fig. 1b).
Histology
The implant-containing bone specimens
were dehydrated in increasing grades of etha-
nol. Thereafter, samples were embedded in
methylmetacrylate (Technovit 7200 VLC-re-
sine, Heraeus Kulzer, Dormagen, Germany).
Longitudinal sections 30–40mm thick were
obtained with a diamond band-saw and a
grinding system (Exakt Apparatebau, Nor-
derstedt, Germany) (Donath & Breuner
1982). The sections were stained with a
modified von Kossa silver method (Hahn
et al. 1992), which selectively shows
mineralized structures at a staining depth
of 1mm.
Histomorphometry
Ground sections of the maxillary tuberos-
ities at the mid-plane level of each implant
were selected for the histomorphometric
analysis. Low-power microphotographs
were made using a Nikon Microphot FX
(Nikon, Tokyo, Japan) and an Agfa colour
transparency film. Then, the colour slides
were scanned with a Nikon L-IV scanner
and stored in a TIFF format on a computer.
The images were imported in the Olympus
MicroImage 3.0 program (Olympus,
Tokyo, Japan) and transformed into binary
images (Fig. 2). The thickness of the peri-
implant area was limited to 0.75 mm from
the internal surface of the screw of the
implant. The entire peri-implant area, the
periapical area (fifth apical area which in-
cluded the semicircular area that sur-
rounded the implant) and the area of the
pericylinder area (implant cylinder area
resulting from subtracting the periapical
area to the entire peri-implant area) were
measured by customized software (Micro-
Image 3.0) (Fig. 2). After that, the trabecu-
lar bone area was measured in each of those
regions, and the bone density was calcu-
lated in each of them. According to Parfitt
et al. (1987) and Ulm et al. (1999), the bone
density was characterized by the trabecular
bone volume, which was defined as the
area of the bone trabeculae as a percentage
of the entire area analyzed (bone area/
analyzed area). The host cancellous bone
area was measured subtracting the thin
cortical bone layers, and the implantFig. 1. Radiographic images of the maxillary tuber-
osity prior (a) and after (b) implant placement.
Blanco et al . Implant placement using osteotome and conventional technique
506 | Clin. Oral Impl. Res. 19, 2008 / 505–510 c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard
and peri-implant areas to the maxillary
tuberosity ground section (Fig. 2); then,
the bony trabeculae were measured and
the bone density was calculated as a per-
centage of bone area/analyzed area.
Statistical analysis
All statistical data were performed through
the use of SPSS 12.0 for Windows (SPSS
Inc., Chicago, IL, USA). Mean values and
standard deviations were calculated for the
host cancellous maxillary bone and for the
entire peri-implant, periapical and pericylin-
der areas. To detect statistical differences,
we applied the Student t-test for paired-
samples observations. Differences were con-
sidered significant when P-values �0.05.
Results
Statistical data of the histomorphometric
measurements of the host cancellous max-
illary bone and of the peri-implant areas are
shown in Table 1. Statistical analysis
(Table 2) confirmed that there was no
significant difference between the host
cancellous maxillary bone density of the
left and right maxillary tuberosities.
Comparison of the peri-implant area andthe host cancellous maxillary bone (Table 2)
The statistical analysis showed that with
the drilling technique there was no differ-
ence between bone densities of the host
cancellous bone and of the entire peri-
implant area. Nonetheless, the percentage
of trabecular bone in the entire peri-im-
plant area is significantly higher with the
osteotome technique. When analyzing the
results by regions, it was found that with
the drilling technique there are no differ-
ences between the apical or pericylinder
areas and the host trabecular maxillary
bone. It was observed that with the osteo-
tome technique there were no statistical
differences in bone densities between the
pericylinder area and the cancellous max-
illary bone; nevertheless, when comparing
the host cancellous maxillary bone with
the periapical area it was observed that
bone density in the periapical area was
significantly greater.
Comparison between osteotome andconventional techniques (Table 2)
The histomorphometric study demon-
strated that the bone density of the entire
peri-implant area was significantly greater
with the osteotome technique than with
the conventional drilling technique (Tables
1 and 2). When peri-implant bone was
analyzed by zones (apex and cylinder
areas), it was observed that the periapical
bone density was also significantly greater
with the osteotome technique (53.32�12.26) in comparison with the conven-
tional drilling technique (34.18� 6.34).
However, when comparing both techni-
ques for bone density achieved in the peri-
cylinder area the difference was no
significant, although it was slightly higher
for the osteotome group (32.3� 8.74) than
for the drilling technique (30.34� 7.2).
Peri-implant regionalization (Table 2)
No significant difference was found be-
tween the periapical area (34.18� 6.34)
and the pericylinder area (30.34� 7.2) in
terms of bone density when using the
drilling technique. On the contrary, with
Fig. 2. Microphotographs of implants placed in the maxillary tuberosity with standard (a), and osteotome (b)
techniques. (c, d) Binary images obtained with the Olympus Microimage 3.0 of the standard (c) and osteotome
(d) techniques. Pericylinder areas were marked with yellow lines. Periapical areas were marked with cyan
lines. The boundaries of the cancellous maxillary bone are marked with orange lines.
Table 1. Percentage of trabecular bone in the peri-implant area and in the host cancellous maxillary bone (mean values� standarddeviations)
Entire peri-implant Periapical Pericylinder Host cancellous maxillary bone
Conventional technique 31.06 � 5.9 34.18 � 6.34 30.34 � 7.2 31.9 � 6.61Osteotome technique 39.38 � 9.67 53.32 � 12.26 32.3 � 8.74 32.19 � 6.27
Blanco et al . Implant placement using osteotome and conventional technique
c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard 507 | Clin. Oral Impl. Res. 19, 2008 / 505–510
the osteotome technique, there was a
greater significant amount of trabecular
bone at the periapical area (53.32�12.26) compared with the pericylinder
area (32.3� 8.74). This proved that the
condensation of the maxillary bone trabe-
culae by means of osteotomes is not pro-
duced in a homogeneous way all along the
implant surface, because it was detected
only in the periapical area.
Discussion
The osteotome technique was introduced in
oral implantology with the aim of improv-
ing primary stability, as well as increasing
the success rate in clinical situations of
poor quality bone, i.e., the posterior max-
illa (Summers 1994a). In theory, osteo-
tomes for bone condensation (tapered
osteotomes) provide the possibility of
achieving improved primary stability of
the implant in cancellous bone through
radial reinforcement of the bone. Thus,
the higher survival rate of oral implants
placed with osteotomes for bone condensa-
tion has been attributed to an enhancement
of the primary stability of the implant due
to the lateral osseocompression of the peri-
implant trabecular bone (Summers 1994a,
1994b, 1995; Fernandez & Fernandez
1997; Komarnyckyj & London 1998;
Nocini et al. 2000). Nevertheless, in the
posterior maxillae of human cadavers
our study showed that with Straumann’s
tapered osteotomes, the bone condensation
is only significant in the fifth apical area.
Therefore, new experimental data, as re-
moval torque test or resonance frequency
analysis, are required to assess whether this
increase implies an improvement of the
primary stability of implants in the poster-
ior maxilla of human cadavers.
The currently available experimental
data in animals do not provide a clear
answer on the clinical value of the osteo-
tome technique. Ex vivo studies in mini-
pigs and goats have reported different re-
sults. After placing titanium implants in
the mandible of minipig, Buchter et al.
(2003) found a statistically significantly
better primary bone anchorage with the
conventional technique than the osteo-
tome technique. Nonetheless, Shalabi
et al. (2006) found no significant differ-
ences between the two techniques in the
femoral condyle of goats, but demonstrated
higher removal torque values for the so-
called undersized preparation technique.
Experimental in vivo studies in rabbits
and minipigs have also reported controver-
sial results. In the distal femoral condyle of
rabbits, Nkenke et al. (2002) found a higher
percentage of bone to implant contact in
the early phases of healing after placing the
implants with the osteotome technique,
although at 8 weeks this significant differ-
ence no longer existed. The authors stated
that the osteotome technique increases
new bone formation and leads to an en-
hanced osseointegration of dental implants
in trabecular bone. In partially edentulous
maxillae of minipigs (Nkenke et al. 2005b),
higher bone to implant contact values were
achieved for implants placed with the os-
teotome technique that were loaded either
immediately or after healing periods of 1–3
months, but no significant differences in
the implant survival rate were shown be-
tween immediate and early functional load-
ing for either of the two techniques (Nkenke
et al. 2005a). After healing periods of 4–5
months, implant site preparation with spiral
drills showed slightly better results. None-
theless, experiments in the cranial and cau-
dal tibia of minipigs showed significantly
higher removal torque values and bone to
implant contact ratios in the early phases of
healing for the standard technique compared
with the osteotome protocol (Buchter et al.
2005a, 2005b).
The discrepancies observed in animal
models may be attributed to differences in
loading conditions, healing times and the
density of the bone selected for the inves-
tigation, i.e., the mandible of the minipig
has a more compact bone than the femoral
condyle of the rabbit. It is important to
mention that the osteotome technique
should not be used systematically in all
types of bone. Strietzel et al. (2002) re-
ported that the use of the osteotome tech-
nique in good quality bone (types 1 and 2)
produces more bone resorption than the
standard technique. This may be due to
the higher forces for bone compression
applied in the compact bone. If much force
Table 2. Statistical analysis of the bone density (paired samples t test)
P-value
Host cancellous maxillary bone (left) – host cancellous maxillary bone (right) 0.666Comparison of the peri-implant area and host trabecular boneHost cancellous maxillary bone (left) – entire peri-implant area (ST) 0.332Host cancellous maxillary bone (left) – periapical implant area (ST) 0.304Host cancellous maxillary bone (left) – pericylinder implant area (ST) 0.109Host cancellous maxillary bone (right) – entire peri-implant area (OT) 0.001n
Host cancellous maxillary bone (right) – periapical implant area (OT) 0n
Host cancellous maxillary bone (right) – pericylinder implant area (OT) 0.944Comparison between conventional and osteotome techniquesEntire peri-implant area (ST) – entire peri-implant area (OT) 0n
Periapical implant area (ST) – periapical implant area (OT) 0n
Pericylinder implant area (ST) – pericylinder implant area (OT) 0.146Peri-implant regionalizationEntire peri-implant area (ST) – periapical implant area (ST) 0.081Entire peri-implant area (ST) – pericylinder implant area (ST) 0.39Pericylinder implant area (ST) – periapical implant area (ST) 0.123Entire peri-implant area (OT) – periapical implant area (OT) 0n
Entire peri-implant area (OT) – pericylinder implant area (OT) 0n
Pericylinder implant area (OT) – periapical implant area (OT) 0n
nSignificant difference.
ST, standard or conventional technique; OT, osteotome technique.
Blanco et al . Implant placement using osteotome and conventional technique
508 | Clin. Oral Impl. Res. 19, 2008 / 505–510 c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard
is used to insert implants, the trauma on
the bone will cause more bone resorption
and osseointegration will take more time
(Abrahamsson et al. 2004).
Recently, systematic reviews and meta-
analysis of clinical studies estimated that
after 24–36 months (Emmerich et al. 2005)
and after 4–5 years (Shalabi et al. 2007a),
the survival rate of implants placed using
the osteotome technique, with and with-
out sinus floor elevation, seems to be
similar to that of implants placed using
conventional drilling techniques. Never-
theless, when oral implants were placed
in the maxillary tuberosity, the osteotome
technique may be chosen as it has two
main advantages: (a) the osteotomes in-
stead of sharp drills minimize the surgical
complications, mainly the hemorrhage
from the palatine artery (Fernandez &
Fernandez 1997); (b) when the osteotome
technique is combined with the use of
implants with more-bioactive implant sur-
face (TPS and SLA), the need of bi-cortical
anchorage into the pterygoid processes is
reduced, thus diminishing the risk of tuber
fracture (Nocini et al. 2000).
Finally, we would like to remark that
actually implant surface is as much impor-
tant as the surgical technique in clinical
survival rate. Experimental data showed
that new implant surfaces, such as the
SLA (Sandblasted, Large grit and Acid-
etched), promote greater osseous contact
at earlier time points (Cochran et al. 1998;
Abrahamsson et al. 2004; Szmukler-
Moncler et al. 2004; Shalabi et al. 2007b).
In summary, the results showed that the
osteotome technique achieved a greater
significant amount of trabecular bone in
the fifth apical region of the peri-implant
area (periapical area). A small increase in
bone density was observed in the periapical
area when implants were placed with the
standard technique but this increase was
not significant.
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