Joe Merheb The fate of buccal bone around dental

Marjolein Vercruyssen
Wim Coucke
implants. A 12-month postloading
Ludovic Beckers follow-up study
Wim Teughels
Marc Quirynen

Authors’ affiliations: Key words: bone resorption, bone thickness, buccal bone, implant
Joe Merheb, Marjolein Vercruyssen, Wim Teughels,
Marc Quirynen, Unit of Periodontology,
Department of Oral Health Sciences, University Abstract
Hospital Leuven & University of Leuven, Leuven, Introduction and aim: Buccal bone thickness is considered to be an important factor during
Belgium
implant surgery. Its resorption might have an effect on the soft tissue stability and eventually on
Wim Coucke, Scientific Institute of Public Health,
Brussels, Belgium implant survival. This study aimed to investigate the resorption of the buccal bone over the first
Ludovic Beckers, UNI-DENT & Elysee Dental, 12 months after implant loading.
Leuven, Belgium
Materials and methods: Twenty-four subjects (47 implants) were included. The buccal bone
Wim Teughels, Marc Quirynen, Research group
Periodontology & Oral microbiology, Department thickness was measured during implant surgery at several distances from the implant shoulder
of Oral Health Sciences, University of Leuven, using a specifically designed device which allows buccal bone thickness measurements without the
Leuven, Belgium
elevation of a muco-periostal flap. These measurements were repeated after 12 months of loading.
Corresponding author: Sixteen implants were placed flapless and 31 with the elevation of a flap. Of the latter, 19 were
Joe Merheb placed following a one-stage protocol and 12 following a two-stage protocol.
Department of Periodontology
Faculty of medicine Results: The mean reduction in buccal bone thickness, when all groups pooled, was 0.26, 0.36,
KU Leuven 0.35 and 0.27 mm at the shoulder and 2, 4 and 6 mm apically. Implants with initial bone thickness
Kapucijnenvoer 33 3000 <1mm (thin buccal plate) did not lose significantly more bone than those with an initial thickness
Leuven, Belgium
Tel.: 0032 16 332409 ≥1mm (thick bone plate) except in the ‘open-flap, one-stage’ group (P = 0.009). A flapless
Fax: 0032 16 332484 procedure leads to less bone resorption compared to an open-flap procedure (P = 0.03). However,
e-mail: joe.merheb@uzleuven.be
the number of surgeries (one stage vs. two stages) did not influence the rate of bone resorption
(P = 0.23).
Conclusion: Within the limitations of this study, one might question the necessity of having a
thick bone plate at the vestibular site of the implant.

Date:
Accepted 19 November 2015
To cite this article:
Merheb J, Vercruyssen M, Coucke W, Beckers L, Teughels W,
Quirynen M. The fate of buccal bone around dental implants.
A 12-month postloading follow-up study.
Clin. Oral Impl. Res. 28, 2017, 103–108.
doi: 10.1111/clr.12767
Osseointegration in its early days was consid-
ered to be an exceptional event. This implied
that both the clinician’s and patients’ expecta-
tions were rather low and the restoration of
function was the primary goal. However, the
situation nowadays is different. Advance-
ments both in the clinical and in the scientific
field have led to a rise in the expectations and
the definition of success is gradually drifting
toward a situation of perfect esthetic and func-
tional mimicking of the natural dentition.
Because of its expected influence on the
state of the soft tissues, the buccal bone plate
has been the subject of different investiga-
tions. Several authors have suggested that the
buccal plate facing a dental implant should
have a minimal thickness of 1 mm (Belser
et al. 2008), while others have recommended a
minimal thickness of 2 mm (Spray et al. 2000;
Buser et al. 2004; Grunder et al. 2005). These
claims have, however, remained undocu-
mented, and most recommendations have
been based on experts’ opinion rather than on
solid scientific data. One widely referred study
(Spray et al. 2000) has tried to investigate the
influence of initial buccal bone thickness on
bone resorption. While its number of included
patients is impressive (above 2600 subjects),
the deductive analyses and the conclusions
raised some questions. A critical review on
the importance of buccal bone thickness can
be found in two systematic reviews (Teughels
et al. 2009; Merheb et al. 2014). Other studies
with more strict protocols unfortunately only
report on observations that did not extend
beyond the stage of abutment placement,
when a flap was reflected and direct measure-
ments were possible (Cardaropoli et al. 2006).
The aim of this study was to investigate
the influence of initial buccal bone thickness
facing an implant at installation on the buc-
cal bone remodeling and bone loss up to

© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 103
Merheb et al
Buccal bone around implants
12 months after implant loading. This study
also aimed to investigate the influence of
some aspects of the surgical protocol on this
buccal bone remodeling.
Material and methods
Patients selection
This study was conducted at the Department
of Periodontology of the University Hospitals
of the Katholieke Universiteit Leuven (Leu-
ven, Belgium). After approval of the study
protocol by the University’s ethical commit-
tee, 33 subjects (64 implants) were recruited
among patients consulting the hospital seek-
ing treatment by means of dental implants.
The study was carefully explained to the
patients, and their informed consent was
taken. To be included in the study, patients
needed to be generally healthy, refrain from
heavy smoking (<10 cigarettes/day), have no
contraindications for implant placement and
have the clinical indication for bilateral
placement of implants in either the maxillary
or mandibular anterior region (premolar to
premolar). Patients were excluded from the
study if the clinical and radiological examina-
tion indicated that additional guided bone
regeneration (GBR) or other grafting proce-
dures were indicated. Additional inclusion
and exclusion criteria can be found in
Table 1. In each patient, one or two implants
(in different quadrants) were selected.
Table 1. Inclusion and exclusion criteria
Inclusion criteria
1. Provision of informed consent
2. Bilateral partial or full edentulism
3. In need of 2–8 implants in the maxilla or
mandible
4. A history of edentulism in the area of
implant treatment of at least 6 months
Exclusion criteria
1. Unlikeliness to comply with study
procedures
2. Untreated, uncontrolled caries and/or
periodontal disease
3. Known or suspected current malignancy
4. History of chemotherapy within 5 years
prior to surgery
5. History of radiation in the head and neck
region
6. History of other metabolic bone diseases
7. A medical history that makes implant
insertion unfavorable
8. Need for systemic corticosteroids
9. Current or previous use of intravenous
bisphosphonates
10. Current or previous use of oral
bisphosphonates for more than 3 years
11. History of bone grafting and/or sinus lift in
the planned implant area
12. Current need for bone grafting and/or sinus
lift in the planned implant area
13. Present alcohol and/or drug abuse
104 | Clin. Oral Impl. Res. 28, 2017 / 103–108
Nine patients had to be excluded from the
study:
Two patients dropped out of the study
before the implant placement surgery.
Three patients had received cemented
constructions which therefore could not
be removed at the 1-year follow-up
(n = 6 implants).
Three patients did not wish to come to
the 1-year follow-up appointment.
(n = 5 implants).
One patient had to be excluded because of
an error in the manipulation of the mea-
suring needles which rendered the data
unusable. (n = 2 implants).
The population pool was thereafter reduced
to 24 subjects with 47 implants.
The patients were randomly assigned (ran-
dom draw) to either:
• ‘F0’: The ‘flapless’ group where implants
were placed without raising a muco-peri-
ostal flap, with the help of a mucosa or
tooth supported surgical guide. Healing
abutments were placed during the same
intervention. (n = 8 patients, 16 im-
plants).
• An ‘open-flap’ group where implants were
placed in conjunction with raising a
muco-periostal flap along the vestibular
plate (n = 16 patients, 31 implants). The
‘open-flap’ group was further divided into
two subgroups:
o ‘F1’: The ‘open-flap, one-stage’ group
where healing abutments were placed
in the same intervention as the
implants (n = 10 patients, 19 im-
plants).
o ‘F2’: The ‘open-flap, two-stage’ group
where healing abutments were placed
during a second surgery, after osseoin-
tegration had taken place (6 months).
This group included the implants
which showed a lack of primary stabil-
ity and where it was considered safer
to allow a submerged healing of the
implants (n = 6 patients, 12 implants).
Description of measurement device
A mechanical device was manufactured (Lab
UNI-DENT & Elys
ee Dental, Leuven, Bel-
gium) to allow the measurement of bone
thickness without reflection of a mucosal
flap. The measuring device is composed of an
L-shaped metallic structure soldered to a
metallic abutment specific for the implant
system (ASTRA TECH Implant System,
DENTSPLY Implants). The rectangular part
of the measuring device had four cylindrical
© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
sleeves at levels corresponding to the implant
shoulder and at 2, 4 and 6 mm more apically.
The sleeves were just large enough in diame-
ter to allow the introduction of a blunt nee-
dle (diameter: 0.6 mm, length 25 mm)
without any lateral movement (Fig. 1).
Surgical procedure and thickness
measurements
Each of the included subjects received two to
six implants bilaterally in either the maxilla
or the mandible (ASTRA TECH Implant Sys-
tem, DENTSPLY Implants). The implants
were placed according to the standard manu-
facturer’s guidelines, using either mental nav-
igation or a stereolithographic surgical guide.
In every subject, two implants (the most ante-
rior implant of each quadrant) were selected
for evaluation. In one subject, only one
implant was selected because guided bone
regeneration was unexpectedly needed on the
other. After implant placement, the measur-
ing device was screwed on top of the implant
and the measurements (at each of the four
previously described levels) were performed in
duplicate. The distances from the endodontic
stopper to the top of the needle were mea-
sured using an electronic caliper. This mea-
sure was then subtracted from the known,
previously measured, distance to the implant
surface. The difference of the two measures
corresponded to the buccal bone thickness
(Fig. 1). For the first eight patients in whom
flap surgery was performed, measurements
were also performed after replacing the flap,
to assess the influence of soft tissues interpo-
sition on the accuracy of the measurements.
After a period of osseointegration of 6 months
(in all three groups), the patients received the
final prosthetic rehabilitation. Measurements
were repeated 12 months after rehabilitation.
Statistical analysis
Descriptive statistics were calculated on an
implant level. A regression line between buc-
cal bone thickness at different times was cal-
culated, and its intercept and slope were
compared with the 45° line. Intercepts and
slopes where also compared between the dif-
ferent surgical protocols (groups: F0, F1 and
F2). Dependence between data was modeled
by integrating the patient as random factor in
the model.
In addition, a linear mixed model with the
patient as random factor was fit to compare
the bone loss over time between initial bone
thickness groups (≥1 mm or <1 mm) and
between the different surgical protocols
(groups F0, F1 and F2). P-values were cor-
rected for simultaneous hypothesis testing
 Merheb et al
Buccal bone around implants

thickness less than 1 mm and 88.3% of all

(a) (b)
implants had a buccal bone thickness less
than 2 mm (Table 2).
The average initial buccal bone thickness
at implant placement was the lowest at the
implant shoulder level (1.1 mm) and became
larger at more apical levels. No differences in
the distribution of the initial buccal bone
dimensions were found between the different
subgroups (Table 3).

Buccal bone resorption up to 12 months after

implant loading
(c) (d)
Twelve months after implant loading, 70.2%
of the implants showed a buccal bone thick-
ness of less than 1 mm and 93.6% of the
implants had a buccal bone thickness of less
than 2 mm at the implant shoulder (Table 2).
If all implants groups were considered (F0,
F1 and F2, n = 47), on average the buccal
bone thickness decreased with 0.31 mm
between implant placement and the 12-
month postloading follow-up (Table 3).
In the ‘open-flap, two-stage’ group (F2,
Fig. 1. Measuring device and protocol. (a) Measuring device and measuring levels. (b) Device placement and mea- n = 12), on average and over the four mea-
suring technique (on model). (c) Device placement and measuring technique (on patient). (d) Use of digital calliper surement levels, the buccal bone thickness
for thickness calculation.
decreased 0.29 mm between implant inser-
tion and abutment placement and of
0.37 mm between insertion and the 12-
Table 2. Distribution of buccal bone thickness (%)
month postloading follow-up (Table 3).
0–0.5 mm 0.51–1 mm 1.01–2 mm >2 mm A minimal decrease of 0.08 mm was
Insertion (n = 47) recorded at implant shoulder level between
Shoulder 40 16.7 31.7 11.7
abutment placement and the 12-month post-
2 mm 13.3 21.7 46.7 18.3
4 mm 11.9 20.3 39 28.8 loading stage (group F2, n = 12).
6 mm 10.6 12.8 40.4 36.2 A comparison of the change in buccal bone
Abutment (n = 12) thickness over 12 months, at shoulder level,
Shoulder 41.6 33.3 16.6 8.3
showed no significant difference between the
2 mm 16.6 25 41.6 16.6
4 mm 8.3 8.3 50 33.3 initially thin (<1 mm at implant shoulder)
6 mm 8.3 16.6 33.3 41.6 and thick (>1 mm at implant shoulder) buc-
12 months (n = 47) cal bone plates (P > 0.05), except for group
Shoulder 51.1 19.1 23.4 6.4
2 mm 14.9 31.9 36.2 17 ‘F1’ between the moments of insertion and
4 mm 12.8 14.9 48.9 23.4 the 1-year follow-up (Table 4). Post hoc anal-
6 mm 8.5 6.4 38.3 46.8 yses revealed that in order for the differences
to reach significance with a reasonable
chance, in between 96 implants (F0, Insertion
according to Sidak. Residual analysis of the made both while the buccal muco-periostal – 1Y) and 17,202 implants (F2, Insertion – 1Y)
linear mixed model showed no deviations flap was reflected and after it was replaced should have been included.
from normality. A P-value below 0.05 was and sutured. This allowed the assessment of A comparison of the change in buccal bone
considered to be significant. the influence of soft tissues interposition on thickness over 12 months showed no differ-
Finally, a post hoc analysis was performed the accuracy of the measurements. On aver- ence in the resorption extent between the
to determine the number of implants that age, the absolute difference between the one-stage (F1) and two-stage (F2), open-flap
this study would have needed to include in respective measurements was 0.08 mm groups (P = 0.23). However, less resorption
order to detect a significant difference. (SD = 0.06, range [0.01; 0.18]) and did not was observed (Insertion – 1Y) when no flap
reach significance (P = 0.20). was raised (F0) compared to when the flap
Results was raised once (F1) (P = 0.03) or twice
Initial bone dimensions (P = 0.02). Post hoc analyses revealed that in
Accuracy of measurements and influence of The empirical cumulative distribution of ini- order for the difference between groups F1
flap interposition tial buccal bone thickness at the implant and F2 be significant with a reasonable
For the first eight patients in whom a flap shoulder level showed that 56.7% of all chance (less for F1) 280 implants should have
was raised, buccal bone measurements were implants investigated had a buccal bone been included.

© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 105 | Clin. Oral Impl. Res. 28, 2017 / 103–108
Merheb et al
Buccal bone around implants

Table 3. Average buccal bone thickness and changes towards observation at implant insertion (mean  SD and median)
S (0 mm)* 2 mm 4 mm 6 mm
Measuring level Group Mean  SD Median Mean  SD Median Mean  SD Median Mean  SD Median
Initial thickness (mm) (n = 47 at insertion 0FL 1.17  0.87 1.08 1.82  0.91 1.81 2.09  0.86 2.05 1.88  1.41 1.94
1Fl 1.09  0.69 1.14 1.96  0.73 1.98 2.16  0.95 2.1 2.06  1.29 1.62
2Fl 1.02  0.84 0.91 1.99  0.88 2.02 2.25  0.93 2.35 2.11  1.27 2.19
Average 1.1  0.77 0.93 1.92  0.79 1.78 2.16  0.91 2.01 2.01  1.3 1.91
Abutment connection (n = 12) 2Fl 0.82  0.58 0.82 1.58  0.95 1.21 1.88  0.97 1.76 1.94  1.05 1.74
Twelve months of loading (n = 47) 0FL 0.98  0.72 0.69 1.64  0.74 1.59 1.82  0.96 1.88 1.71  1.66 1.44
1Fl 0.79  0.66 0.63 1.53  0.72 1.46 1.80  0.81 1.61 1.73  1.81 1.56
2Fl 0.77  0.73 0.70 1.5  0.83 1.4 1.81  0.94 1.7 1.8  1.77 1.87
Average 0.85  0.71 0.72 1.56  0.75 1.39 1.81  0.93 1.65 1.74  1.72 1.55
*
S: Implant shoulder level.

Table 4. Influence of initial bone thickness on subsequent bone resorption prosthetic reconstruction. The results show a
Bone thickness Group Stages considered Difference P-Value relative dimensional stability even for ini-
Thin–thick F0 S - 1Y 0.28 0.14 tially thin (<1 mm) buccal plates. It also
Thin–thick F1 S - 1Y 0.92 0.009 showed that the major part of the bone
Thin–thick F2 S - 1Y 0.09 0.89 resorption takes place during the initial heal-
Thin–thick F2 S - Ab 0.31 0.23
ing phase. Scatter plots between the abut-
Thin–thick F2 Ab - 1Y 0.25 0.15
ment placement phase and the 12-month
Thin: buccal plate <1 mm; thick: buccal plate ≥1 mm; F0: flapless; F1: open-flap, one-stage surgery; follow-up stage show that buccal bone thick-
F2: open–flap, two-stage surgery; S: surgery; Ab: abutment placement; 1Y: one-year postloading fol-
low-up; a negative value in the ‘difference’ section indicates more resorption in the first mentioned ness remains roughly constant, suggesting
group (Thin). Bold value indicate P < 0.05 that most of the bone remodeling occurs in
the initial 4 months healing phase and that
buccal bone stabilized thereafter (Fig. 2). The
measurements made between the implant
insertion and the 12-month postloading fol-
4

low-up show a dimensional stability of the

buccal plate.
3

There seems to be no difference in buccal

Abutment

bone resorption between the thick and the

1Y
2

thin buccal plates except for the open-flap,

one-stage group (F1). This particularity could
possibly be attributed to the rather limited
1

sample size. It is, however, noteworthy that

thin buccal plates lost in absolute values
0

more bone that thick buccal plates. This dif-

0 1 2 3
Insertion
Fig. 2. Scatter plot of buccal bone thickness at insertion against abutment placement (group 2Fl) and abutment
placement against the 1 year post loading follow up.
At the 12-month follow-up, in the initially
thin plate group, two implants showed an
absence of buccal bone at the shoulder level.
At the subsequent levels (2, 4, 6 mm), all the
implants showed the presence of a buccal
bone plate. In the initially thick group, one
implant showed the absence of bone at the
shoulder level and at the 2- and 4-mm levels.
Those differences were found to be nonsignif-
icant (P > 0.05).
Discussion
Various authors have claimed that an initial
buccal bone thickness of 2 mm is necessary
4 0 1 2
Abutment
for the preservation of the buccal bone plate.
It was hypothesized that a thin buccal plate
is less resistant to the different types of
trauma an implant can endure and would
therefore be more prone to resorption and
buccal implant exposition. In consequence,
this exposition could lead to a higher rate of
complications and failures. In a case series
followed up to 10 years, Buser et al. (2013)
showed that implants placed with a concomi-
tant GBR to recreate a thick bone plate,
achieved a high dimensional stability over a
long period of time. The current study fol-
lowed 24 patients over a period of 1.5–
2 years, of which the end point was
12 months after placement of the definitive
3 4 ference, however, did not reach significance.
A significant difference in amount of
resorption is detected between the flapless
and open-flap procedures. These results are
in accordance with the results of fundamen-
tal studies (Wilderman 1967) which conclude
that flap elevation lead to a bone resorption
from the surgical trauma of up to 0.4 mm.
However, our study did not find a significant
difference in the amount of resorption if the
flap was raised once or twice (groups F1 vs.
F2). This observation suggests that buccal
bone resorption might be more of a conse-
quence of the remodeling process following
implant placement and general trauma (dril-
ling, lateral pressure, presence of a foreign
body) inflicted during implant placement sur-
gery and which could affect bone resorption
over the whole ridge. This hypothesis is in
accordance with the observations made after
tooth extraction and which indicate a total
volumetric change of the alveolar ridge even

106 | Clin. Oral Impl. Res. 28, 2017 / 103–108 © 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

though no flap is raised (Araujo & Lindhe
2005). The discrepancy between the two
above-mentioned results might suggest that
little to no remodeling happens in a second
phase after initial bone remodeling has taken
place following implant placement and/or
flap elevation. Nevertheless, these results are
to be interpreted with much caution because
the limited size of group ‘F2’ (n = 12) might
increase the probability for a statistical error
and be the real explanation of the observed
discrepancy.
Computerized tomography has demon-
strated that in the incisor region, the buccal
bone plate around a tooth was thinner than
1 mm in 86% of the cases (El Nahass &
Naiem 2015). Most such cases would lead to
a GBR simultaneously to implant placement.
Guided bone regeneration is a predictable
intervention. It, however, implies higher
costs for the patient, higher postoperative dis-
comfort and swelling (Urban & Wenzel
2010), a higher complication rate (Bazrafshan
& Darby 2014) and a slightly higher failure
rate (Chiapasco & Zaniboni 2009). Long-term
dimensional stability of thin buccal plates
might allow avoiding some of the GBR proce-
dures leading to a simplified treatment. Even
though this study seems to indicate that
implants with a thin buccal bone do not lose
more bone than implants surrounded by a
thick buccal bone plate, it should not be for-
gotten that in both cases, bone resorption
still occurs. One can deduce that a moderate
bone resorption of a razor sharp buccal plate
might more easily induce bony dehiscences
and potentially esthetical impairments than
a bony resorption of the same extent of a
thick buccal plate. Therefore, it is important
to note that the present study is not advocat-
ing the placement of implants in very thin
bone without concomitant bone regeneration
but rather questions the need for extremely
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thick bony plates around dental implants and
its esthetical impact. In this study, the cutoff
value was set at 1 mm. To better address the
question of whether a 2-mm buccal bone
plate was necessary or not, this cutoff value
would have better been set at 2 mm. How-
ever, the very limited number of buccal bone
plates which were initially >2 mm (11.7%)
rendered this analysis irrelevant as its results
would have been very questionable from a
statistical perspective.
The present study used physical measure-
ments and calipers to evaluate plate thick-
ness and thickness changes. This method
might suffer from slight imprecisions which
could intervene at the moment of intra-oral
direct measurement or at the moment of
extra-oral caliper measurement. Additionally,
measurements could have been flawed by
intra-observer and interobserver variability.
Part of these imprecisions has been handled
by double measurement at each site, but
interobserver variability was not addressed.
The presence of soft tissues might also have
had an impact on the precision of the mea-
surements. However, measurements per-
formed on eight patients after flap elevation
and then after the flap was replaced showed
an absolute discrepancy of 0.08  0.06 mm,
which was considered acceptable by the
authors of this study. The design of the
device allowed measurements to be per-
formed at the implant shoulder and also 2, 4
and 6 mm apically of the shoulder. Even
though measurements at all levels were per-
formed, the measurements at 6 mm were
excluded from later calculations as the opera-
tors found that the interference of the buccal
vestibulum and anatomical structures, such
as the lip, might have flawed the precision of
the measurements. Additionally, in the pre-
sent study, only ASTRA TECH implants
with an Osseospeed surface were used. This
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Buccal bone around implants
implant has a moderately rough, fluoride-
modified surface. A fluoride-modified surface
has been demonstrated to enhance bone
retention and bone preservation (Ellingsen
et al. 2004; Berglundh et al. 2007) through
the enhancement of trabecular bone density
and the promotion of collagen inclusion in
the bony matrix (Shteyer et al. 1977; McCor-
mack et al. 1993). It is not known whether
similar results with thin buccal plates would
be achieved with other available surfaces. It
should also be noted that the different groups
show unequal size. This is due to the rather
limited sample size. This discrepancy is,
however, purely cosmetic and does not affect
the validity of the randomization process
(Schulz & Grimes 2002).
The current results advocate a simplifica-
tion of the implant treatment by suggesting a
more stringent selection of the cases requir-
ing a bone augmentation. However, for such
results to be confirmed, further investiga-
tions should be conducted on a larger pool of
subjects with a longer follow-up (up to
5 years). Additionally, a systematical mea-
surement of bone thickness levels at the
moment of loading (which was not performed
in this study) to better understand the
chronological pattern of bone resorption
should be made. Finally, a recording of the
gingival biotype and the amount of kera-
tinized mucosa (Bengazi et al. 2014) which
are known to affect the extent of postsurgical
bone resorption is advised. It is essential that
these factors and possibly others be taken
into account in upcoming studies.
Acknowledgement: Dental implants
and abutments were provided, free of charge
by DENTSPLY Implants (M€ olndal, Sweden).
& Belser, U.C. (2013) Long-term stability of
early implant placement with contour augmen-
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182S.
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