Liene Molly Bone density and primary stability in

implant therapy

Authors’ affiliations: Key words: bone implant interface, bone regeneration, clinical assessment, diagnosis,
L. Molly, Department of Periodontology, Catholic
guided tissue regeneration, morphometric analysis, structural biology, tissue physiology
University of Leuven, Leuven, Belgium
L. Molly, Department of Periodontology, University
of Maryland, Baltimore, MD, USA Abstract
Correspondence to: Introduction: To improve patient comfort, deviations from the very successful standard
L. Molly osseointegration protocol are being developed. To keep implant failure rates as low as
University of Maryland
possible, the most perfect treatment planning and a good patient selection are extremely
650 W Baltimore Street
Baltimore MD 21201 important. Because bone density plays an important role in implant outcome, known
USA relations of bone density could improve treatment planning.
Tel.: þ 1 410 70671452
Fax: þ 1 410 7063028 Material and methods: A Pubmed search revealed 66 manuscripts investigating and
discussing bone density of human jawbone whether or not related to implant stability or
outcome. Forty-five of these will be discussed in this review.
Results and discussion: Many pre-operative methods of jawbone density assessment are
available. Most of those techniques correlate well with one another. Some are more
elaborate to use in clinical practice. Primary stability measurements show significant
correlations with different bone densities and also with implant outcome; however, not
many studies investigate both at the same time.
Conclusion: To investigate the outcome of adaptation methods of the surgical protocol
with regard to the jawbone density, an objective pre-surgical determination of bone
density is necessary.

To cite this article:
Molly L. Bone density and primary stability in implant
therapy.
Clin. Oral Imp. Res., 17 (Suppl. 2), 2006; 124–135
r 2006 The Authors
Journal compilation r Blackwell Munksgaard 2006
It is necessary to indicate that this review
paper investigates the assessment of bone
density rather than bone quality. Many
papers in the literature define bone quality
as equivalent to bone density. This cannot
be taken for granted because many more
factors are important when investigating
bone quality than bone density alone. Bone
metabolism, cell turn over, mineralization,
maturization, intercellular matrix, vascular-
ity and others are very important in the
definition of bone quality and eventually
may very well influence implant outcome.
The extent to which every single factor of
bone quality, as stated above, influences the
outcome of the implant treatment, has not
yet been defined. Large epidemiological stu-
dies will be necessary to investigate this.
Therefore, this review will only address one
factor of bone quality, namely bone density.
Bone density seems to be of great im-
portance not only in primary implant sta-
bility but also in the predictability of oral
implant outcome.
Following the standard osseointegration
protocol, P-I Brånemark put forward, very
high success rates can be obtained; up to
99% cumulative success rates are reported
in the interforaminal region of the lower
jaw (Lindquist et al. 1996).
In this standard protocol, two-stage sur-
gery is a prerequisite, leaving the implant

124

submerged for 3–6 months, depending on
the region of interest where the implants
are placed. This should allow primary os-
seointegration. At the time point of unco-
vering, the bone-to-implant contact (BIC)
ratio should be high enough to allow a load-
bearing superstructure to be successfully
placed and maintained. Many different
biological factors are contributing to the
failure of osseointegration of oral implants
(Esposito et al. 1998). The authors con-
cluded that surgical trauma and anatomical
conditions are the most important factors
for primary implant losses; jawbone qual-
ity, volume and overload are major deter-
minants for late implant failures. The
impact of these factors on implant failure
rate depends on the implant design and
surface characteristics and can be altered
by modifying the surgical technique. Jaffin
& Berman (1991) and Herrmann et al.
(2005) stated that poor bone quantity and
especially poor bone quality are the main
risk factors for implant failure using
this standard protocol. One can figure
when deviations from this protocol take
place; this risk factor becomes even more
important.
Primary osseointegration did not take
place yet when, e.g. early or immediate
loading is applied and in these instances
primary stability will be a major issue.
Primary implant stability can be mea-
sured at implant placement using several
biomechanical devices.
The relation between biomechanically
measured primary stability and pre-surgical
measurements of bone density could help
in treatment planning. An adaptation of
the surgical technique, the loading protocol
or design and surface characteristics of the
implant could improve.
The aim of the present review is to:

present the different methods of bone
density measurements available for
clinical use and to investigate whether
their validity has been tested.

Present the different methods of im-
plant stability assessment available
for clinical use and to investigate
their validity in effectively testing
implant stability as defined in this
chapter. This will include assessment
of the predictive value of insertion
torque measurements on implant out-
comes.

Verify whether there is any relation
indicated in the literature between pri-
mary stability and bone density.

Investigate whether there is any rela-
tionship indicated in the literature be-
tween bone density and treatment
outcome.
Material and methods
Search strategy
A first Medline (Pubmed) search was per-
formed to identify all articles investigating
bone density. The search was restricted
from 1988 till January 1, 2006. Because
in the literature bone density has always
been referred to as bone quality, the follow-
ing search parameters have been included
in the search: ‘assessment of bone quality
in human jaw bone’, ‘surgical protocol’ and
‘jaw bone quality’. This search revealed
66 results. For all of these manuscripts,
abstracts were screened for inclusion to
answer one or more of the questions
addressed in the aims. Forty-five of the
screened manuscripts were selected for
further investigation. The manuscripts
that were not selected discussed the rela-
tion between bone density and extrac-
tion difficulties during the third molar
extraction and between bone density and
the surgical treatment of cleft palate/
alveolar ridge patients. The selected manu-
scripts were divided into four different
groups according to the questions posed in
the aims of the review.
Group 1 contained all articles discussing
a method of bone density measurement
and/or assessing their validity. Eleven arti-
cles were selected. To extend this search,
related articles of the selected manuscripts
were also screened for inclusion. In this
group, only two articles were included in
the discussion of this topic based on the
relevance in answering the posed question.
In the results, a table has been constructed
to clarify the scientific relevance of each
paper included.
Group 2 contained all articles discuss-
ing methods of primary implant stability
measurements and their validity. Sixteen
articles were selected. To extend the
search, related articles of the selected
manuscripts were also screened for inclu-
sion. In this group, four articles were
selected from this extended search. In the
125 |
Molly . Bone density and implant stability
results, a table has been constructed to
clarify the scientific relevance of each pa-
per included.
Group 3 contained all articles verifying a
correlation between primary stability and
bone density. Eight articles were selected to
be discussed in this group. In this case,
screening of related articles did not reveal
further manuscripts suitable for inclusion.
In the results, a table has been constructed
to clarify the scientific relevance of each
paper included.
Group 4 contained the articles discussing
the adaptation of the surgical protocol re-
lated with bone density. In this group, 10
articles were selected. Research of the
manuscripts related to the ones selected
revealed selection of five more articles.
Again, in the results, a table has been
constructed to clarify the scientific rele-
vance of each paper included.
Results and discussion
Pre-operative methods of jawbone density
assessment
The golden standard for bone density measure-
ments has been considered as the histological
and morphometrical measurement of the
jawbone
Small biopsies taken pre-operatively can be
used for histomorphometric evaluation.
Trephine biopsies can be histologically pre-
pared, ground, sliced and stained to allow a
calculation of the percentage of bony tra-
beculae over the total biopsy area. This
technique was compared with the subjec-
tive perception of bone density by the
surgeon during the preparation and place-
ment of oral implants (Trisi & Rao 1999).
The surgeon was able to detect extremely
dense bone and extremely soft bone but
could not distinguish any other bone den-
sities. Comparison of 3D-obtained mor-
phometric data through micro-computed
tomography (mCT) with previously taken
conventional CT images from human ca-
daver mandibles and maxillae revealed a
general agreement between both, stating
higher bone density in the mandibles vs.
the maxillae and in the anterior areas vs.
the posterior (Fanuscu & Chang 2004).
The mCT technique can give more speci-
fied information on trabecular thickness
and trabecular separation but is more time
consuming and is not possible on in vivo
subjects.
Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135
Molly . Bone density and implant stability
Quantitative-computerized tomography (qCT)
measurement of the jawbone
qCT is the most frequently used method to
measure the density of the spine in the
diagnosis of osteoporosis in females. Ob-
jects with a known density are situated on
the same radiograph and allow a compar-
ison with the tissues to investigate. The
ten 2-mm-thick vertical CT slices perpen-
dicular to the buccal and lingual plates of
15 mandibles were investigated according
to this technique (Lindh et al. 1996). Ante-
rior sections showed higher values than
posterior sections, and a huge intra- and
intersubject variation was present.
Implementing an aluminum step-wedge
in the radiograph taken is based on the
same principle. Some researchers have im-
plemented such a wedge in intra-oral radio-
graphs to measure bone density (Southard
et al. 2000; Nackaerts et al. 2006). They
were originally investigating the relation
between jawbone density and general ske-
leton bone density measured through dual
energy X-ray absorptiometry (DEXA) (see
further) in the radius.
Nobel price winner Hounsfield (1980)
described the quantitative calibration in
Hounsfield units, now frequently used in
all medical fields, in 1980. This X-ray
attenuation unit is mostly used in com-
puted tomographic scanning and charac-
terizes the relative density of a substance.
Each pixel is assigned a value between  1
and 1 k. The value of zero equals water,
and soft tissue such as muscle tissue equals
þ 40, air (  1000) and bone ( þ 50 to
þ 2500). Quantitative cone beam-compu-
terized tomography (qCBCT) was com-
pared with qCT (Aranyarachkul et al.
2005). Both techniques used Hounsfield
units to score bone density. The correlation
between both techniques was very signifi-
cant; the ratings of the qCBCT were, how-
ever, higher than for the qCT method,
which means an overestimation of bone
density when using the cone beam method.
This should of course be taken into con-
sideration when performing implant plan-
ning using the qCBCT radiographic
visualization.
DEXA scan measurements of the jawbone
The DEXA technique to measure bone
density is frequently used to characterize
fracture risk in large epidemiological stu-
dies. The precision of DEXA in human
126 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135
jawbone was investigated in 1999 (Denis-
sen et al. 1999). Small trephine biopsies of
the human jawbone were prepared, 10
stored in alcohol and 10 histologically
treated, and investigated on bone mineral
density by DEXA. The coefficients of var-
iation are comparable with those of precise
qCT measurements. This DEXA method
could thus replace pre-operative qCT mea-
surement of bone density in case no CT is
necessary of the area of interest. No other
studies using DEXA as a bone density
analysis of human jawbone could be re-
trieved from the Pubmed search. The paper
by Becker et al. (2000) suggests that DEXA
measurements of the peripheral bones (ra-
dius and ulna) do not gain any beneficial
information on bone density at the site of
implant placement. In this study, the
sample size was too small to identify a
relation between peripheral osteoporosis
and implant loss.
Magnetic resonance imaging (MRI) of the jaw-
bone
Thin slice high-resolution MRI was used
for bone density and quantity assessment
to allow proper implant planning in mand-
ibles and maxillae (Gray et al. 1996). This
technique can be used in patients where
the use of ionizing radiation is contra
indicated. So far, no publication could be
found investigating the validity of deter-
mining bone density through MRI.
Ordinal bone density classification of the jaw-
bone based on panoramic and cephalometric
radiographs
In 1985, Lekholm & Zarb described a
classification method to pre-operatively
score bone density based on panoramic
radiographs. This classification was used
worldwide because it is easy to use and
does not involve a huge investment. Bass
& Triplett (1991) showed in their results on
1097 investigated Brånemark implants in
303 jaws which bone density graded as four
exhibited the greatest failure rate. Herr-
mann et al. (2005) came to the same
finding. They investigated 487 sites, of
which only 3% showed bone density,
four combined with an unfavorable anat-
omy. Jaffin & Berman (1991) also found a
high failure rate (35%) in type 4 bone. All
studies investigate bone density relation
with implant outcome when implants
were placed according to the standard
protocol.
A significant relation was detected be-
tween bone mineral density (single-energy
CT) of the mandibular cortex and an ordi-
nal classification (1–3) of the morphology
of the inferior cortex based on panoramic
radiographs (Klemetti & Kolmakow 1997).
This finding may be interesting in implant
planning but a more specified classification
is more elaborate when bone quality be-
comes more important in the planning, e.g.
when immediate loading is applied.
Table 1 will clarify the impact of all studies
discussed in this part of the discussion.
Pre-operative assessment of implant
stability
Stability is generally defined as ‘a measure
of the difficulty of displacing an object or
system from equilibrium.’ In clinical
terms, however, ‘primary’ stability is not
clearly defined, but is commonly under-
stood as a lack of implant movement im-
mediately after placement.
The three most frequently used methods
to gain an understanding of bone density
during implant placement are based on
biomechanical bone properties. The devices
s
used are Periotest (Medizintechnik, Gul-
s
den, Bensheim, Germany), Osstell (Inte-
gration Diagnostics, Gothenburg, Sweden)
s
and Osseocare (Nobel Biocare, Gothen-
burg, Sweden). Another method could be
the subjective scoring of the surgeon using a
pre-determined classification as mentioned
earlier (Trisi & Rao 1999).
s
Periotest measurements
s
The Periotest device is a tapping device
that measures the braking point when tap-
ping the implant surface (Aparicio et al.
2006). Aparicio (1997) reported on 1182
Brånemark implants inserted consecutively
in 315 patients and followed for 8 years,
measuring PTVs at several time intervals.
The two most important findings were the
correlation of PTV post-operatively and
secondary failure and the possibility of
early detection (before fabrication of the
superstructure) of a failing implant.
While the single PTV measurement has
been shown to correlate (only descriptive
statistics) with the ordinal bone density
classification, there is as yet no evidence
that it provides valid means to define
primary stability (Lekholm & Zarb 1985;
 Table 1. Pre-operative methods of jawbone density assessment
Authors Publication Type of the study Number of Question addressed Result
date subjects
Trisi & Rao 1999 Prospective 56 Correlation of ordinal classification of bone Interclass correlation analysis of variance investigated the difference
quality with histomorphometric bone of one class with the overall score of data sets, it showed that classes
density D1 (P ¼ 0.01) and D4 (P ¼ 0.0006) were significantly different from the
total population, the clinical classes D2 (P ¼ 0.6) and D3 (P ¼ 0.4) were
not significantly different
Fanuscu & Chang 2004 In vitro cadaver humans Correlate micro CT with conventional CT General agreement between mCT and qCT was not noted
Lindh et al. 1996 15 Correlation of qCT with bone mineral density Anterior mandible revealed higher values than posterior ones
(BMD) (Po ¼ 0.05) and the variations between the mandibles was
statistically significant (P ¼ 0.0001). This was investigated for qCT
measurements and compared with the BMD histological, both
showed the same results
Nackaerts et al. 2006 In vitro cadaver humans 47 Correlation between DEXA bone The correlation coefficient between the aluminum equivalent values
measurements and aluminum equivalent of and the areal BMD results of the DXA scan was 0.81 (Po0.001)
intra-oral X-rays measuring the BMD of the
same bone sample
Southard et al. 2000 Prospective CT 41 Relation between bone density in the The density of the maxillary alveolar arch was most strongly related
alveolar arches and other bone areas, to the density of the mandibular alveolar process (P ¼ 0.0006) but
e.g. hip there was no relation found with other areas through DEXA
measurements
Hounsfield 1980 In vitro Descriptive method of measuring bone Descriptive method
density through gray values on CT images
Aranyarachkul et al. 2005 In vitro cadaver humans 9 Correlation between qCT and qCBCT A very high correlation between qCT and qCBCT (r ¼ 0.92–0.98) was
discovered
Denissen et al. 1999 In vitro cadaver humans 20 Correlation between mineral density and A very high correlation between DEXA density measurements and
DEXA density measurements of trephine histomorphometric measurements could be detected (r ¼ 0.9995)
biopsies
Becker et al. 2000 Cohort study 98 The relation between osteoporosis and No substantial associations between pDEXA bone density scores and
implant failure implant failures were observed (r ¼ 0.71–1.23, Po0.5)
Gray et al. 1996 Descriptive study 12 Description of the MRI technique to visualize Descriptive method
bone anatomy and density
Bass & Triplett 1991 Retrospective CT 274 The correlation between implant outcome There was no significant difference found in implant outcome
and jaw bone anatomy, implant location and between the different scorings for jaw bone anatomy according to

127 |
age at implant placement the Lekholm & Zarb classification, there was a significant statistically
better outcome for implants placed in the anterior lower jaw
compared with the posterior lower jaw restored with fixed
restorations (X2 ¼ 0.0001) and no difference could be found in
implant outcome between the different ages at implant placement
Herrmann et al. 2005 Retrospective CT 487 implants Identification of prognostic implant failures Bone quality 4 according to the Lekholm & Zarb classification was the
jawbone quality with the highest failure rate (P ¼ 0.00013)
Jaffin & Berman 1991 Retrospective CT 1054 implants Relation between bone quality according to Only descriptive statistics are available because of the low failure rate
the Lekholm & Zarb classification and
implant outcome
Klemetti & 1997 In vitro cadaver humans The correlation between the BMD of the The changes in the mandibular cortex were significantly related to
Kolmakow mandibular cortex and the ordinal the BMD of the buccal cortex (P ¼ 0.002)
classification of the morphology of the
inferior cortex on panoramic radiographs

CT, computed tomography; mCT, micro-computed tomography; qCT, quantitative-computerized tomography; DEXA, dual energy X-ray absorptiometry; qCBCT, quantitative cone beam-computerized
tomography; MRI, magnetic resonance imaging.

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135

Molly . Bone density and implant stability
Molly . Bone density and implant stability
Truhlar et al. 1994). Furthermore, there is
at present no evidence that the single report
s
of a measurement using the Periotest
device provides any predictive value of
implant outcome.
s
Osstell measurements
Meredith et al. (1996) first published on
their new resonance frequency device de-
veloped to investigate the height of the
implant not surrounded by bone and the
stability of the implant/tissue interface
(Aparicio et al. 2006).
A high correlation (r ¼ 0.84, P  0.05)
was found when comparing the mean tor-
que values of the upper/crestal portion with
the resonance frequency values at implant
placement (Friberg et al. 1999a, 1999b).
MkIV Brånemark implants, however, in-
serted in low-quality bone show a lower
insertion torque and higher resonance fre-
quency than standard Brånemark implants.
This translates into better primary stability
with a reduction of the energy imparted
into the bone at the implant site (O’Sulli-
van et al. 2004a, 2004b). Many authors
correlated these resonance frequency mea-
surements to deviations from the standard
protocol. If these resonance frequency mea-
surements can be related with pre-treat-
ment determined bone quality, these
correlations become very interesting for
pre-treatment outcome prediction and
eventual altering of the protocol. However,
at present, no evidence that the single
s
report of a measurement using the Osstell
device during implant placement provides
any predictive value of implant outcome.
s
Insertion torque measurements (Osseocare )
The use of cutting resistance measure-
ments to assess bone density during im-
plant surgery was first described by
Johansson & Strid (1994). The technique
involved the measurement of torque cre-
ated when cutting a thread in a hole in bone
as determined by the current drawn by an
electric motor. A decomposition procedure
was applied to eliminate torque compo-
nents resulting from frictional forces and
shiver packing during the tapping course,
which, according to the authors, resulted in
a true profile of cutting resistance. Bone
quality was expressed as the energy re-
quired to remove a unit volume of bone,
and for cortical bovine bone an in vitro
measurement of 0.3 J/mm3 was quoted.
128 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135
Other workers have measured insertion
torque in N cm during placement of
implants in pre-tapped sites (Ueda et al.
1991) or when placing self-tapping im-
plants (Friberg et al. 1999a, 1999b, 2003;
Johansson et al. 2004). Insertion torque in
pre-tapped sites differs from thread-cutting
forces measured with a screw tap or a self-
tapping implant. The major variable influ-
encing insertion torque when a threaded
implant is inserted into a pre-tapped hole in
bone is the relative tolerance of the thread
profile of the tap and the implant fixture. If
thread-cutting forces are excluded, then
insertion torque is a function of the com-
pressive stresses applied locally to the sur-
rounding bone and friction at the implant–
bone interface. Moreover, many authors
have used the peak insertion torque value
as an indication of primary implant stabi-
lity. For a parallel-walled Brånemark type
of implant, the peak value is generated
when the implant head is seated in the
marginal bone. For tapered implant de-
signs, a continuous increase of insertion
torque can be seen as a result of lateral
compression during insertion (O’Sullivan
et al. 2000). The relationship between true
cutting resistances insertion torque and
peak insertion torque is presently not clear.
High correlations between PTVs and in-
sertion torque force (R value  0.74579)
for 75 implants installed in 12 fresh bovine
ribs were also described (Tricio et al. 1995).
There is as yet, however, no evidence that
insertion torque measurment provides a
valid means to define primary stability.
Three studies that evaluated the prog-
nostic value of insertion torque measure-
ments to predict future implant failure
were found. Friberg et al. (1999a, 1999b)
followed 523 Brånemark implants for 3
years, of which 412 were subjected to
cutting torque measurements. Comparison
of the insertion torque values for 14 failed,
and 398 successful implants did not reveal
any statistically significant differences. Si-
milar results were obtained by Johansson et
al. (2004), who used the same technique to
evaluate 222 Brånemark implants placed in
grafted and non-grafted maxillae and fol-
lowed for 1 year. There was no difference
between 28 failed and 194 successful im-
plants with regard to initial cutting torque
value. A recent study, however, comparing
the survival of immediately (test) or de-
layed (control) loaded single-tooth restora-
tions on Frialit-2 implants, showed a
statistically significant increase in implant
success for the immediate-loaded implants
if the insertion torque was higher than
20 N cm (Ottoni et al. 2005). The relative
risk for implant failure was associated
with insertion torque for the test group
where implants were loaded immediately
(r ¼ 0.79, P  0.007).
Clinical studies on immediate implant
loading have been using a predetermined
level of insertion torque as an inclusion
criterion (Hui et al. 2001; Calandriello
et al. 2003; Malo et al. 2003; Vanden
Bogaerde et al. 2003; Östman et al. 2005).
These authors also used a modified surgical
technique to improve initial stability by a
combination of thinner drill diameters,
osteotomes, wide-platform implants and
tapered implants. Although survival rates
were high, the importance of high insertion
torque for the outcome is not known.
Concerns have been forwarded that a high
insertion torque may lead to overcompres-
sion and negative tissue effects. However,
Calandriello et al. (2003) could not see any
influence of torque (15–52 N cm) on mar-
ginal bone levels after 1 year in function.
Table 2 will clarify the impact of all studies
discussed in this part of the discussion.
Relation of primary stability with bone
density
The study of Truhlar et al. (1994) com-
pared PTVs in the different categories of the
ordinal classification of Lekholm & Zarb
(1985). The investigators found mean
PTVs at second-stage surgery of  3.82 
3.04 for type 1,  3.7  3.06 for type 2,
 3.3  3.2 for type 3 and  1.29  3.57
for type 4 quality bone. Another group
correlated the same techniques and their
results show a different change of PTVs
over time in densities 1 and 2 compared
with 3 and 4, which could indicate a better
bone-to-implant contact over time in better
bone densities (Morris et al. 2003). A
similar finding was published in Truhlar
et al. (2000); these authors added that
hydroxyapathite-coated implants became
less stable over time in contrast with non-
coated implants, which showed an im-
provement in stability over time. However,
PTV values at implant placement and
thereafter should be better correlated with
an objective bone density classification to
obtain more specified information.
 Table 2. Per-operative assessment of primary stability
Authors Publication Type of the Number of Question addressed Result
date study subjects
Trisi & Rao 1999 Prospective 56 Correlation of ordinal classification of Interclass correlation analysis of variance investigated the difference of one
bone quality with histomorphometric class with the over all score of data sets, it showed that classes D1 (P ¼ 0.01) and
bone density D4 (P ¼ 0.0006) were significantly different from the total population, the
clinical classes D2 (P ¼ 0.6) and D3 (P ¼ 0.4) were not significantly different
Aparicio 1997 Retrospective CT 315 The relation of the PTV at implant The percentage of secondary failures (implant outcome) was related to the
insertion with different implant initial PTV corresponding to a borderline implant (only descriptive statistics)
characteristics, e.g. implant outcome
Meredith 1996 In vitro Verify if resonance frequency analysis can Resonance frequency analysis is reproducible (better than 1%) and there is a
et al. give an idea of the bone tissue interface strong correlation (Po0.01) between the exposed height of an implant above
and the bone level surrounding the mimicking bone and resonance frequency in vitro
implant
O’Sullivan 2004a, 2004b Prospective CT 13 The correlation of bone quality and The mean insertion torque for type IV bone according to the Lekholm & Zarb
et al. implant stability classification was significantly different statistically from other types of bone
for (P ¼ 0.05). No difference correlated with the type of bone could be found for
the different implant types in this study
Johansson 1994 In vitro cadaver 42 Correlation between cutting resistance of A linear correlation could be found represented in a graph
& Strid animals the bone and the aluminum-referred
density form X-ray assessment
Ueda et al. 1991 In vitro cadaver 2 Relationship between insertion torque Removal torque was lower than insertion torque but no statistical analysis was
humans and removal torque available
Friberg et al. 1999a, 1999b Prospective CT 105 The correlation between cutting torque A high correlation was found between the insertion torque encountered at
values and radiographically and clinically implant placement and the bone quality assessments (descriptive statistics)
assessed bone quality scores
Friberg et al. 1999a, 1999b Prospective CT 9 Implant stability comparisons at implant The insertion torque encountered during the first part of implant insertion was
insertion using resonance frequency and highly correlated with the resonance frequency measurement at implant
insertion torque placement (r ¼ 0.84, Po0.05)
Friberg et al. 2003 RCT 44 The relation between primary and Resonance frequency at implant insertion was significantly higher (P ¼ 0.004) in
secondary implant stability and the 1 year the test than in the control group. As for implant outcome there was no
outcome of the implants with two difference between test and control (P ¼ 0.48)
different surfaces
O’Sullivan 2000 In vitro cadaver 9 Correlation of primary stability of five The peak insertion torque encountered during insertion of MkIV is significantly
et al human different implant types higher (Po0.05) compared to the insertion torque encountered during
insertion of standard Brånemark implants, MkII and oxidized titanium implants.

129 |
The resonance frequency measured after insertion of MkIV implants was
statistically significant better (Po0.05) compared with standard Brånemark
implants
Tricio et al. 1995 In vitro cadaver 12 The correlation between PTV There was a statistically significant correlation between the insertion torque
animals measurements and insertion torque force and PTVs (R ¼  0.75) and between the mean gray values of the selected
during implant insertion and gray value area around the implants and PTVs (R ¼  0.83)
around the implant
Johansson 2004 RCT 40 The correlation between cutting Significantly higher torque values were required for placing implants in
et al. resistance and bone grafting particulate grafts (one stage) used in inlay grafts than for block grafts (two
stage) used in only grafts (Po0.001). A strong correlation between insertion
torque measurements and the estimates of bone quality according to the
Lekholm & Zarb classification was found (Po0.001)
Ottoni et al. 2005 RCT 23 The relation between failure rate and The relative risk for implant failure was associated with insertion torque for
insertion torque in immediate and implants in the group of immediate loading (r ¼ 0.79, P  0.007)
delayed loaded implants
Calandriello 2003 Prospective CT 26 The relation between primary stability or Statistical analysis could not reveal relation between bone quality, bone
et al. bone quality and quantity and marginal quantity or insertion torque and marginal bone loss or implant outcome

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135

Molly . Bone density and implant stability

bone loss or implant outcome

 Molly . Bone density and implant stability

Single resonance frequency analysis P  0.001). A manuscript defining a strong

measurements were evaluated at different correlation between computerized tomo-
time points after implant placement with graphy values (Hounsfield values) and
Descriptive article of the technique of immediate provisional restoration

the ordinal Lekholm & Zarb classification
of bone density measured on panoramic
radiographs (Zix et al. 2005). This study
did not find any significant relation and
suggested that a follow-up over time of the
RFA values could elucidate better relations.
There was no statistical difference found at any time
the cutting torque values encountered
during implant placement (correlation
coefficient ¼ 0.77, P ¼ 0.01) was published
in 2005 (Ikumi & Tsutsumi 2005). When
implant torque values were compared with
the subjective scorings based on radio-

Huang et al. (2002) tried to correlate RFA
with different bone densities using finite
element analyses to mimic different bone
qualities. RFA was computed with differ-
ent bone types and bone densities. Their
Only descriptive statistics available
Only descriptive statistics available
graphs according to the ordinal classifica-
tion of Lekholm & Zarb (Johansson et al.
2004), only classes 2, 3 and 4 were de-
tected. Lower torque forces were encoun-
tered when inserting the implant into type

results show a linear decrease in RFA
values with a decrease in bone density.
These results must be interpreted with
caution concerning the non-isotrophic
character of bone in vivo. The relation
between resonance frequency measure-
ments over time and bone density mea-
sured according to the ordinal Lekholm &
Result
4 bone, not only for the first part of implant
insertion but also for the middle and last
part. As for analysis of early implant out-
come, the insertion torque forces for suc-
cessfully osseointegrated implants were
higher than for the failures. Whenever in-
sertion torque shows correlation with pri-
mary oral implant stability or with

Zarb classificiation based on radiographs prediction of implant outcome, a sugges-

was investigated (Barewal et al. 2003). tion for adaptation of the surgical technique
The resonance frequency measurements can be possible.
overtime in immediately loaded implants
measurements at implant insertion and

were performed at surgery and every week Table 3 will clarify the impact of all studies
and implants loaded according to the
Comparison in resonance frequency

thereafter up to 6 weeks after surgery. The discussed in this part of the discussion.
lowest resonance frequency measurement
was found at 3 weeks for all groups of bone Possible adaptation methods of the
density. The decrease in resonance fre- surgical protocol with regard to jawbone
quency was the largest in the group with density
Follow-up over time
Follow-up over time
Follow-up over time
Question addressed

bone density graded as 4 (8.6%); in the Before starting this discussion, one must be
standard protocol

same group, the increase between weeks
3 and 6 in resonance frequency was the
largest of all groups (26.9%). These differ-
ences between groups were, however, only
statistically significant for groups 1 and 4
bone density at the 3-week follow-up. This
Number of
aware that in the literature, many studies
were conducted to compare two techniques
but only a few proved that the difference
between both techniques is really due to
the low or high bone densities present.

is probably again due to the subjective Adaptation of the surgical technique

subjects

origin of the classification method used. Several papers suggest the use of osteo-
CT, computed tomography; RCT, randomized-controlled trial.
24
76
36

20

Insertion torque measurements retrieved tomes in the placement of oral implants

from 31 implants placed in 10 human in the posterior maxilla or maxillary tuber-
cadaver jawbones were compared with mi- osity (Komarnyckyj & London 1998; No-
Prospective CT
Prospective CT
Prospective CT

Prospective CT
Type of the

croradiographical bone density analysis and cini et al. 2000; Toffler 2001). Most papers
morphometric analysis (Friberg et al. only suggest the low bone density in the
study

1995). A statistically significant relation region of interest but do not test the bone
was found between the peaks of bone density. Toffler (2001), when investigating
density retrieved from the microradio- the use of osteotomes with internal sinus
Publication

graphs and the peaks of insertion torque elevation, even concludes that histological
retrieved from implant placement for each and clinical comparisons for the traditional
2001
2003
2003

2005
date

implant site (r ¼ 0.90, P  0.001). Another lateral sinus elevation were lacking. Roc-
Table 2. Continued

statistically significant relation was found cuzzo & Wilson (2002) published a manu-
Östman et al.

for the correlation between total bone area script on the use of acid-etched implant
Malo et al.

Bogaerde

surrounding the inserted implant measured placement in combination with the use of
Hui et al.
Authors

Vanden

morphometrically on microradiographs and osteotomes in preparation of the implant

et al.

the mean cutting resistance values occur- site. They also suggested that the bone in
ring during implant insertion (r ¼ 0.74, the posterior maxilla has a poor quality. In

130 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135

 Table 3. Relation between primary stability and bone density
Authors Publication Type of the Number of Question addressed Result
date study subjects
Truhlar et al. 1994 Retrospective 1838 implants Correlate PTV with bone density Descriptive statistics
CT
Lekholm & Zarb 1985 Descriptive Set-up of a classification Description of a classification
Morris et al. 2003 In vitro Verification if different PTV in different bone Descriptive statistics
densities occurs
Truhlar et al. 2000 Prospective CT 2900 implants Correlation of PTV with bone quality The differences in the changes in the PTVs for each bone quality were
measurements defined by the Lekholm & statistically different (Po0.001, Hotelling’s Trace). Non-coated implants show
Zarb classification better PTV values than HA-coated implants (Po0.038, Hotelling’s Trace)
Zix et al. 2005 Retrospective 35 Correlation between resonance frequency No statistically significant correlation could be found between the resonance
CT values and the type of bone present frequency at implant placement and the type of bone present
Huang et al. 2002 In vitro Is it possible to develop a technique to define Description of a finite element analysis model in the detection of resonance
resonance frequency of an implant before frequency in vitro during implant planning, a significant linear relationship was
implant placement found in vitro (Po0.0001)
Barewal et al. 2003 Prospective CT 20 The correlation between resonance The only difference in resonance frequency measurements was observed
frequency measurements and the kind of between implants inserted in types 1 and 4 bone (P ¼ 0.004), after 5 weeks no
bone available based on the Lekholm & Zarb more differences could be observed
classification for bone quality
Friberg et al. 1995 In vitro 10 The correlation between cutting resistance The correlation between the bone density and cutting resistance peaks was
cadaver and bone quality based on highly correlated (Po0.001) and the correlation between total bone area and
human microradiography and morphometric mean cutting resistance values also showed a positive relation (Po0.001)
analysis
Ikumi & Tsutsumi 2005 Prospective CT 13 The correlation between CT values of the A significant correlation between cutting resistance and CT values could be
bone and cutting resistance at implant found (P ¼ 0.01) with correlation coefficient of 0.77
placement
Johnasson et al. 2004 RCT 40 The correlation between cutting resistance Significantly higher torque values were required for placing implants in
and bone grafting particulate grafts (one stage) used in inlay grafts than for block grafts (two
stage) used in only grafts (Po0.001). A strong correlation between insertion
torque measurements and the estimates of bone quality according to the
Lekholm & Zarb classification was found (Po0.001)

CT, computed tomography; RCT, randomized-controlled trial.

131 |
validated.

s
Adaptation of the implant design

s
nance of osseointegration over time.

extracted for microscopic analysis and im-

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135

also showed statistically significant higher
insertion torque values than the standard
assessed with the ordinal Lekholm &
the previously determined bone quality
Tech AB, Molndahl, Sweden) implant and
compare implant outcome was not present.
bone specula; however, no histomorpho-

the MkIV Brånemark implant maintained a

implant and the 3i Osseotite implant, and
showed statistically significant higher peak
radiographs. The MkIV Brånemark implant
In 2000, the initial stability of five different
There is no evidence that the discussed

sessment mostly performed has not been

largest part because the bone density as-
bone density on implant outcome for the
ple can be performed. A control group to
of bone density with a standard bone sam-
cularized connective tissue rich in lamellar
plants were placed. Histology revealed vas-
2003). Six months after the sinus floor
An investigation the role of human re-
follow-up. They conclude that long-term
measurements post-operatively and 1-year
loading based on clinical and radiographic

Brånemark implant, the MkII Brånemark

Zarb classification on the basis of oral
these measurements were compared with
que measurements gave an impression of
the primary stability of the implants and
implant. Peak insertion torque, resonance
frequency measurements and removal tor-
the 3i Osseotite (3i[Implant Innovations
mark implant, the Astra Tioblast (Astra
standard Brånemark implant was compared
man cadavers (O’Sullivan et al. 2000). The
manuscripts have proven the influence of
metry was performed. Thus, no correlation
bone graft was performed (Philippart et al.
ment of bone density of a human calvaria
combinant tissue factor, platelet-rich
follow-up is necessary to observe mainte-
successful primary osseointegration before

augmentation procedure, bone cores were

Molly . Bone density and implant stability

dard Brånemark implant. In type 4 bones,

with the MkII self-tapping Brånemark im-
conclusion, a 6-week healing period allows

resonance frequency values than the stan-

plasma and tetracycline in the improve-

Incorporated], Palm Beach, Florida, USA)

plant, the MkIV-tapered self-tapping Bråne-
implant designs was compared in fresh hu-
 Table 4. Possible adaptation methods of the surgical protocol in regard to jawbone density
Authors Publication Type of Number of Question addressed Result

132 |
date the study subjects
Toffler 2001 Descriptive Description of the technique: apical alveolar Description of the technique
displacement with osteotomes
Nocini et al. 2000 Case report Description of osseous distraction through Description of the technique
the use of osteotomes
Komarnyckyj & 1998 Prospective CT 16 Detecting if the use of osteotomes in sinus A statistically significant difference between the initial situation and the
London elevation procedure is effective situation after bone augmentation by means of osteotomes could be
detected (Po0.01)
Philippart et al. 2003 Prospective CT 18 The use of implants in sinus augmentation Descriptive statistics
procedures
O’Sullivan et al. 2000 In vitro cadaver 9 Correlation of primary stability of five The peak insertion torque encountered during insertion of MkIV is
human different implant types significantly higher (Po0.05) compared with the insertion torque
Molly . Bone density and implant stability

encountered during insertion of standard Brånemark implants, MkII and

oxidized titanium implants. The resonance frequency measured after
insertion of MkIV implants was significantly better statistically (Po0.05)
compared with standard Brånemark Implants
Astrand et al. 2003 Cohort study 40 Evaluating the difference between the MkVI Descriptive statistics

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135

implants and the standard Brånemark
implants
Mordenfeld et al. 2004 Retrospective CT 52 Follow-up over time Descriptive statistics
O’Sullivan et al. 2004a, 2004b Animal study 6 Differences in primary and secondary Only higher resonance frequency measurements could be detected while
stability between tapered and straight using short (6 mm) implants in the tibea when comparing those results at
implants implant insertion for the tapered implants compared with the straight ones
(P ¼ 0.0275). For 10 mm implants no significant statistical difference could be
detected. The implants placed in the femur show a higher insertion torque
for the test implant compared with the control implant (P ¼ 0.0005)
Glauser et al. 2003 Prospective CT 38 Presenting short-term success rate of surface- Descriptive statistics
modified immediate occlusally loaded
implants
Khang et al. 2001 RCT 97 The comparison between two similar Dual acid etched implants were significantly more successful than machined
implants with different surface surfaced implants (Po0.01). No significant statistical relation with bone
characteristics quality according to the Lekholm & Zarb classification could be detected
Iezzi et al. 2005 CT 8 Histological and histomorphometrical Descriptive statistics
analysis of the bone response to submerged
implant inserted in human jaw bone after
certain healing periods
Quirynen et al. 2005 Retrospective CT 539 Find predisposing conditions for peri-apical The incidence of retrograde peri-implantitis was significantly higher
lesions and to evaluate treatment strategies (Po0.0001) for Ti-Unite implants when compared with the machined
implants
Salonen et al. 1997 Retrospective CT 74 Detecting differences between ITI implants No real correlation between ITI and TPS was established; only descriptive
TPS implants statistics were made to verify that
Bass & Triplett 1991 Retrospective CT 274 The correlation between implant outcome There was no significant difference found in implant outcome between the
and jaw bone anatomy, implant location and different scorings for jaw bone anatomy according to the Lekholm & Zarb
age at implant placement classification, there was a significantly better outcome statistically for
implants placed in the anterior lower jaw compared with the posterior
lower jaw restored with fixed restorations (X2 ¼ 0.0001) and no difference
could be found in implant outcome between the different ages at implant
placement

CT, computed tomography; RCT, randomized-controlled trial.


high primary stability in contrast with all
other types tested. The relation between
outcome of tapered MkIV Brånemark im-
plants and soft bone quality was questioned
(Astrand et al. 2003). In a test group,
patients were treated with the tapered
MkIV Brånemark implants and in a control
group the standard MkII Brånemark im-
plants. Investigators suggested a lower
bone quality in the upper jaw. However,
no correlation between bone quality mea-
surements and implant outcome was de-
scribed. The results for both implant
systems do not show any statistical differ-
ence but in the conclusions they do state
that the MkIV implant demonstrates an
improved survival rate compared with ear-
lier results of other Brånemark implants
placed in soft-quality bone.
The survival rate of wide-platform MkII
Brånemark implants in the posterior mand-
ible and maxilla was questioned while sup-
posing that the bone quality in these areas
was lower than in other regions (Morden-
feld et al. 2004). The authors suggested that
wide-platform implants present an accepta-
ble treatment alternative; they, however,
did not set up a true correlation with bone
quality and did not include a control group.
Another study of the group of O’Sullivan
tested the differences in primary stability
for different tapering of implants in rabbit
tibea and femur (O’Sullivan et al. 2004a,
2004b). The insertion torque and resonance
frequency analysis revealed a higher inser-
tion torque for both grades of tapering
compared with the standard Brånemark
implants; the resonance frequency analysis
revealed that it depended on the kind of
bone the implant was inserted in and prob-
ably related to the bone quality, but unfor-
tunately this was not tested.
Adaptation of the implant surface
Glauser et al. (2003) investigated whether
the changed surface characteristics and the
tapered design of the MkVI Ti-Unite
Brånemark (Nobel Biocare, Gothenburg,
Sweden) implants could have a beneficial
effect on immediate loading. Implants were
mainly inserted in soft bone (76%) (Glau-
ser et al. 2003). The bone quality was
measured by the ordinal Lekholm & Zarb
classification based on radiographs. The
outcome of 97.1% after 1 year is high
when compared with other imme-
diate loading studies; however, no control
group was included in this study. PTV
values of ITI (Straumann, Basel, Switzer-
land) implants show higher values than
those of titanium plasma-sprayed implants,
which means a better stability for the rough
surface implants (Salonen et al. 1997).
Two different surface types were placed
in various bone qualities (Khang et al.
2001). The surgeon assessed bone quality
during implant placement using a subjec-
tive classification (dense, normal and soft).
The analysis of implant performance re-
lated to bone quality revealed statistically
significant results. Cumulative success
rates (CSR) at the 4-year follow-up were
93.8% and 87.8% for acid-etched and ma-
chined surface, respectively, in dense bone
quality; as for the soft bone quality, the
CSRs were 96.8% and 84.8%, respec-
tively, which is even far more significant.
Eight implants were retrieved from a hu-
man jawbone with a trephine burr (Iezzi
et al. 2005). All implants were submerged
and unloaded at the time of retrieval; the
reason for retrieval was different in most
cases but was not disintegration. The bone-
to-implant contact varied considerably (30–
90%) but rough surface implants showed a
faster osseointegration on the histological
evaluation. It was extrapolated that rough
surface implants can be loaded successfully
after 2 months even when inserted in soft
bone. The term soft bone was, however,
not defined, and neither was bone quality
assessed before implant placement. The
relation between surface topography and
origin of failure was illustrated (Quirynen
et al. 2005). Ti-Unite Brånemark implants
showed higher retrograde peri-implantitis
than machined surface implants. The over-
all failure rate, however, was considerably
higher for machined surface implants than
for the Ti-Unite implants. The faster pri-
mary osseointegration process achieved
with these modified surface implants thus
allows a lower implant failure rate and a
possibility for early detection of retrograde
peri-implantitis at frequent patient follow-
up visits. This early detection of retrograde
peri-implantitis should be performed
through bone quality comparisons over
time postsurgery.
Adaptation of the loading protocol
Data looking at implant outcome of im-
plants supported with a fixed superstruc-
ture and the correlation with bone quality
133 |
Molly . Bone density and implant stability
based on the ordinal scoring on radiographs
according to the Lekholm & Zarb classifi-
cation showed no statistical difference in
the implant outcome for the different ordi-
nal categories (Bass & Triplett 1991). The
same held true for the implant outcome of
implants supported with a removable
superstructure. This group, however, did
find a significant difference of implant out-
come related to the positioning of the im-
plant in the jaw. These two findings
contradict one another and therefore we
could question the validity of the Lekholm
& Zarb classification in its additional ben-
efit to investigate bone quality effect on
different deviations from the standard
protocol.
There is no evidence that the discussed
manuscripts have proven the influence of
bone density on implant outcome for the
largest part because the bone density as-
sessment mostly performed has not been
validated.
Table 4 will clarify the impact of
all studies discussed in this part of the
discussion.
Conclusion
Many different bone density assessments
are available at the moment. Most of these
show good correlation with one another. In
clinical studies investigating implant stabi-
lity or treatment outcome of different pro-
tocols, however, mostly the subjective
ordinal scoring by means of radiographs is
being used. This scoring showed that it is
only possible to detect extremely soft bone,
which occurs only in 3% of the patients.
This means that less than 1% of the fail-
ures can be detected with this technique. It
was, however, possible to detect that im-
plant stability in soft bone quality shows
the lowest resonance frequency measure-
ments after 3 weeks and that these mea-
surements show extremely increased
values, especially in the soft bone after 6
weeks. To determine specifically, how-
ever, at what stage implants can be suc-
cessfully loaded, more elaborate bone
density detection should be performed.
Histomorphometric techniques show very
good results of correlations between area of
bone present in the vicinity of the implant
and primary implant stability measure-
ments, and bone-to-implant ratio and
Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135
Molly . Bone density and implant stability
primary stability. This technique, how-
ever, implies another surgical intervention
and an extra cost and is thus difficult to
implement clinically. It could, however,
give additional information if correlated
with another technique clinically used in
bone density measurement. An integration
of the newly developed finite element ana-
lysis model (Olsen et al. 2005) in pre-
operative computer planning systems
could help, together with a standardized
qCT (e.g., based on Hounsfield units) clas-
sification, to better understand the relation
of bone density and primary or secondary
implant failure. Based on these results, one
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