Journal of Oral Science & Rehabilitation No. 1, 2017

Journal of Oral Science & Rehabilitation No. 1, 2017

Cover / Editorial / Contents / About the Journal of Oral Science & Rehabilitation / Comprehensive rehabilitation and natural esthetics with implant and orthodontics (CRANIO): An interdisciplinary approach to missing maxillary lateral incisors / Biological and physical properties of bone block grafting biomaterials for alveolar ridge augmentation / Retrospective analysis of periimplantitis therapy of 158 implants / Bone augmentation of canine frontal sinuses using a porous α-tricalcium phosphate for implant treatment / Importance of a preoperative radiographic scale for evaluating surgical difficulty of impacted mandibular third molar extraction / Kinesiographic analysis of lateral excursive movement on the horizontal plane: the retrusive component / Open-cohort prospective study on early implant failure and physiological marginal remodeling expected using sandblasted and acid-etched bone level implants featuring an 11° Morse taper connection within one year after loading / Authors must adhere to the following guidelines / Imprint

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Journal of

Oral Science
&
Rehabilitation
I S S N 2 3 6 5 - 6 8 9 1 (Online)

Volume 3 — Issue 1/2017

I S S N 2 3 6 5 - 6 1 2 3 (Print)

Journal for periodontology, implant dentistry,
dental prosthodontics and maxillofacial surgery

[2] => JOSR_A4_Editorial_03.qxp_Layout 1

Essential Dental Media

Dental Tribune International

The World’s Largest News
and Educational Network
in Dentistry
www.dental-tribune.com

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Editorial

Journal of

Oral Science
&
Rehabilitation

On research and education

Reference
García-Gallego A,
Georgantzís N,
Martín-Montaner J,
Pérez-Amaral T
(How) do research and
administrative duties affect
university professors’
teaching?
Appl Econ.
2015 May 5;47(45):4868–83.

It is well proven that research and education constitute a positive
feedback system. A recent study among 609 university professors
concluded that educators who carry out frequent research activities perform significantly better at their teaching activities.1 This is
equally true when seen from the student perspective. Research is
itself a very powerful educational tool. Being involved in research
activities takes students to a level of critical thinking and in-depth
study that can rarely be achieved with other educational methods.
Even more importantly, science itself would certainly benefit from
the involvement of students in research, as they will always bring
with them fresh and challenging ideas and enthusiasm.
For all these reasons, educational plans and educators should ensure
that undergraduate and postgraduate students have the opportunity
to participate in research activities as early as possible.
Dr. David Peñarrocha Oltra
Associate Editor

Journal of
Oral Science & Rehabilitation

Volume 3 | Issue 1/2017

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Contents

03
Editorial
Dr. David Peñarrocha Oltra
06
About the Journal of Oral Science & Rehabilitation
08
Marco Tallarico et al.
Comprehensive rehabilitation and natural esthetics with implant and
orthodontics (CRANIO): An interdisciplinary approach to missing maxillary
lateral incisors
18
Alberto Monje and Hom-Lay Wang
Biological and physical properties of bone block grafting biomaterials for
alveolar ridge augmentation
32
Jörg-Ulf Wiegner et al.
Retrospective analysis of periimplantitis therapy of 158 implants
44
Masataka Hirose et al.
Bone augmentation of canine frontal sinuses using a porous α-tricalcium
phosphate for implant treatment
52
Natalia Ribes Lainez et al.
Importance of a preoperative radiographic scale for evaluating surgical
difﬁculty of impacted mandibular third molar extraction
60
Andrea Papini et al.
Kinesiographic analysis of lateral excursive movement on the horizontal
plane: the retrusive component
68
Marco Tallarico and Silvio Meloni
Open cohort prospective study on early implant failure and physiological
marginal remodeling expected using sandblasted and acid-etched bone
level implants featuring an 11° morse taper connection within one year
after loading
80
Guidelines for authors
82
Imprint — about the publisher

04 Volume 3 | Issue 1/2017

Journal of
Oral Science & Rehabilitation

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MASTER OF ORAL
IMPLANTOLOGY PROGRAM
San Diego, California

ADVANCED SURGICAL & PROSTHETIC
IMPLANT TRAINING PROGRAM
The advanced surgical & prosthetic Master of
Oral lmplantology Program is designed for
general dentists of all implant experience
levels, as well as specialists in the fields of
prosthodontics, periodontics and endodontics.
The goal of the program is to provide doctors
with the right tools for a successful career in
implant dentistry.
The California Implant Institute and its world-renowned faculty have developed
the most comprehensive curriculum focusing on essential information that is
immediately useful to doctors, their staff, and their patients. Through in-class
interactive lectures, online webinars, hands-on laboratory sessions, live-patient
surgical experiences, and much more, participants will gain the highest level of
knowledge and technical skills necessary to provide safe, appropriate, and
efficient treatments.
Understanding the value of the time invested to complete the Master of Oral
lmplantology Program, CII offers a unique opportunity for doctors to fully
customize their program track to best fit their availability while having the least
impact on their practice.

One-year and two-year tracks available

Training Overview
The Program consists of 7 modules
for a total of 1,000 CE units:
• Didactic / In-Class Lecture Module
Over 60 days of interactive academic learning

• Live-Patient Surgical Module
Perform 30+ surgical implant placements and
20+ bone grafting procedures

• CAD/CAM Computer Guided Module
Hands-on workshop focused on implant surgery

• Implant Prosthodontics Module
Hands-on implant-oriented occlusion workshop
and on-site shadowing of a Prosthodontist

• Hands-On Cadaver Module
• Oral Sedation Certification Module

Visit the CII website for detailed curriculum and schedules.

• Academic and Research Module

Faculty Members
Louie Al-Faraje, DDS

James L. Rutkowski, DMD, PhD

Diplomate, American Board of Oral Implantology
Academic Chairman, California Implant Institute

Diplomate, American Board of Oral Implantology
Past President, American Board of Oral Implantology

Mamaly Reshad, DDS, MSc

Patrick Palacci, DDS

Former Section Chair for Fixed Prosthodontics and
Operative Dentistry, University of Southern California

Christopher A. Church, MD
Diplomate, American Board of Otolaryngology
Director, Loma Linda University Sinus and Allergy

Head of Brånemark Osseointegration Center
in Marseille, France

Domenico Cascione, CDT, B.S.
President of OPERART LLC, a dental laboratory
in Santa Monica, California

www.implanteducation.net
info@implanteducation.net
+1 858.496.0574

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About

About
the Journal of Oral Science & Rehabilitation
The aim of the Journal of Oral Science & Rehabilitation is to promote rapid
communication of scientiﬁc information between academia, industry
and dental practitioners, thereby inﬂuencing the decision-making in
clinical practice on an international level.
The Journal of Oral Science & Rehabilitation publishes original and highquality research and clinical papers in the ﬁelds of periodontology, implant dentistry, prosthodontics and maxillofacial surgery. Priority is
given to papers focusing on clinical techniques and with a direct impact
on clinical decision-making and outcomes in the above-mentioned
ﬁelds. Furthermore, book reviews, summaries and abstracts of scientiﬁc
meetings are published in the journal.
Papers submitted to the Journal of Oral Science & Rehabilitation are subject to rigorous double-blind peer review. Papers are initially screened for
relevance to the scope of the journal, as well as for scientiﬁc content and
quality. Once accepted, the manuscript is sent to the relevant associate
editors and reviewers of the journal for peer review. It is then returned to
the author for revision and thereafter submitted for copy editing. The
decision of the editor-in-chief is made after the review process and is
considered ﬁnal.

About
Dental Tribune Science
Dental Tribune Science (DT Science) is an online open-access publishing
platform (www.dtscience.com) on which the Journal of Oral Science &
Rehabilitation is hosted and published.
DT Science is a project of the Dental Tribune International Publishing
Group (DTI). DTI is composed of the leading dental trade publishers
around the world. For more, visit

www.dental-tribune.com

06 Volume 3 | Issue 1/2017

Journal of
Oral Science & Rehabilitation

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About

Benefits
of publishing in the journal for authors
There are numerous advantages of publishing in the Journal of Oral
Science & Rehabilitation:
– Accepted papers are published in print and as e-papers on
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increased impact of their research through open-access publishing on
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Copyright © 2016 Dental Tribune International GmbH. Published by
Dental Tribune International GmbH. All rights reserved. No part of this
publication may be reproduced, stored or transmitted in any form or by
any means without prior permission in writing from the copyright holder.

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Implant and orthodontic treatment

Comprehensive rehabilitation
and natural esthetics
with implant and orthodontics
(CRANIO): An interdisciplinary
approach to missing
maxillary lateral incisors

Abstract
Background

Marco Tallarico,a Cesare Luzi,b Giorgia Galasso,c
Roberta Lioned & Paola Cozzad
a

Private practice, Rome, Italy; Surgical, Micro-Surgical
and Medical Science Department, University of Sassari,
Sassari, Italy; and Osstem AIC, Italy
b
Private practice, Rome, Italy; and Department of
Orthodontics, University of Ferrara, Ferrara, Italy
c
Orthodontics Postgraduate Training Program, Department of Pediatric Surgery, Bambino Gesù children’s
hospital, Rome, Italy
d
Department of Clinical Sciences and Translational
Medicine, University of Rome “Tor Vergata,” Rome, Italy;
and Department of Dentistry, “Nostra Signora del Buon
Consiglio” University, Tirana, Albania

Corresponding author:
Dr. Marco Tallarico
Via di Val Tellina 116
00151 Rome
Italy

The absence of the maxillary lateral incisors creates a functional and esthetic problem that can be managed with different treatment modalities.
Case presentation

The present case is reported to illustrate an interdisciplinary approach
involving orthodontics and restorative dentistry to manage the case of a
24-year-old Caucasian female with agenesis of the maxillary right lateral
incisor, presence of the maxillary right canine in place of the lateral incisor,
microdontia of the maxillary left lateral incisor, and midline deviation.
Treatment included space opening and positioning of a 3 mm implant
supporting a single-unit crown, placed using computer-assisted, templateguided surgery.
Conclusion

T +39 328 075 8769
me@studiomarcotallarico.it
How to cite this article:
Tallarico M, Luzi C, Galasso G, Lione R, Cozza P.
Comprehensive rehabilitation and natural esthetics
with implant and orthodontics (CRANIO): an
interdisciplinary approach to missing maxillary
lateral incisors.
J Oral Science Rehabilitation.
2017 Mar;3(1):8–16.
08 Volume 3 | Issue 1/2017

Comprehensive interdisciplinary rehabilitation according to the CRANIO
philosophy was effective in successfully restoring function and esthetics
in a young female patient affected by congenitally missing maxillary lateral
incisor.
Keywords

Interdisciplinary treatment, agenesis, dental esthetics, dental implants,
guided surgery.
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Introduction
Congenital tooth agenesis is a common dental
anomaly, with reported incidences of 2.7% to
12.2%, excluding third molars. In the permanent
dentition, maxillary lateral incisors are the most
commonly affected,1 with a prevalence rate of
between 1% and 4%2 and a female predominance of approximately 2:1 compared with
males.3 This anomaly is not usually an isolated
phenomenon, but is associated with other dental anomalies, such as peg-shaped contralateral incisors.1 Therefore, the concurrence of several dental anomalies in the same subject results
in functional and esthetic problems, which may
in turn affect the patient’s self-conﬁdence and
social relationships from a very young age.
Treatment options for missing lateral incisors
include space opening, followed by the placement of a conventional ﬁxed bridge or a single-unit implant-supported crown, and orthodontic space closure with anatomical
recontouring of the canines.4 Selecting the most
appropriate therapy is still a challenge. Numerous clinical characteristics must be analyzed,
such as the patient’s age, occlusal relationships,
proﬁle, smile line, presence or absence of third
molars, and size, shape and color of the canines.5
In order to maximize the esthetic and functional results, an interdisciplinary approach involving an orthodontist, an oral surgeon and a
restorative dentist has become essential. Comprehensive rehabilitation and natural esthetics
with implant and orthodontics (CRANIO) is a
philosophy based on interdisciplinary treatments to achieve stable occlusion and healthy
hard and soft tissue and to enhance the natural
esthetic appearance and subsequent patient
satisfaction.
The aim of the present study was to describe
an interdisciplinary approach to a clinical case
presenting with a missing maxillary lateral incisor treated in two phases: orthodontic space
opening, followed by placement of a narrow
3 mm diameter implant and restored with a
screw-retained lithium disilicate crown veneered on a zirconia abutment.

Case report
A 24-year-old Caucasian female was referred to
our private clinic to seek a second opinion for
treatment, with the chief complaint of an unattractive smile and the mobility of the primary

maxillary right canine. Clinical examination and
radiographs conﬁrmed the advanced root resorption of the primary maxillary right canine,
the agenesis of the permanent maxillary right
lateral incisor, with the presence of the permanent canine in place of the lateral incisor, and
microdontia of the maxillary left lateral incisor
(Figs. 1a–c). Intraoral observation revealed an
Angle Class II relationship of the molars and canine, an increased overjet, a normal overbite and
a lower dental midline that was displaced 3 mm
to the left compared with the upper midline.
Cephalometric analysis (Dolphin Imaging
11.7, Dolphin Imaging and Management Solutions, Chatsworth, Calif., U.S.) highlighted a
mesofacial facial pattern, with a Class II sagittal
skeletal relationship (Fig. 2). The patient presented with a symmetrical and proportional face
and ﬂat facial proﬁle, with the upper lip positioned 4 mm and the lower lip 2 mm behind the
Ricketts E-line.
The previously proposed treatment was extraction of the primary canine with space maintenance for a future implant rehabilitation and
canine substitution with a veneer restoration. In
contrast to this, the alternative treatment proposed was extraction of the primary canine,
followed by orthodontic space recovery for implant placement in the lateral incisal area, with
alignment and leveling of the dental arches. The
option of correcting the Class II relationship
would have required orthognathic surgery,
which was refused by the patient.
The patient was initially very skeptical toward such a comprehensive treatment option.
However, after discussion with both the orthodontist (CL) and implantologist (MT) of the advantages and disadvantages of all of the available treatment options, it became clear to the
patient that the overall advantages of the proposed interdisciplinary treatment, involving orthodontic treatment, implant placement and
prosthetic rehabilitation, would provide improved esthetic and functional results. The disadvantages of the proposed treatment were
related to costs and a longer treatment time.
The orthodontic treatment lasted 18 months.
After the extraction of the primary canine, fullarch bonding with a ﬁxed esthetic multibracket
appliance was performed, and the maxillary
right canine was strategically bonded with a
mesial tip back to enhance root control. Skeletal
anchorage by means of an orthodontic miniscrew (Aarhus System, American Orthodontics,
Sheboygan, Wisconsin, U.S.; 1.5 mm diameter,

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Figs. 1a & b

a

b
Fig. 1c

Figs. 1a–c
Preoperative intraoral view:
frontal (a), right (b) and left (c).
Fig. 2
Cephalometric analysis.

c

Fig. 2

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6.0 mm thread length) was used during canine
retraction with sliding mechanics to avoid side
effects (i.e., worsening of the molar relationship). Both direct and indirect traction to the
miniscrew were used with derotation elastomeric chains for enhanced control of the ﬁnal
crown and root position (Figs. 3 & 4a–c). The

ﬁnishing phase was accomplished with braided
multistrand stainless-steel 0.018 × 0.025 in.
arch wires and intermaxillary elastics. An upper
Hawley plate was used for retention after appliance removal in the maxillary arch, and a mandibular ﬁxed retainer was bonded in the mandibular anterior segment.

Fig. 3

Fig. 3
Periapical radiograph showing
the orthodontic miniscrew.
Figs. 4a–c
Orthodontic treatment:
right (a), left (b)
and occlusal (c) view.

Fig. 4a

a

c
Figs. 4b & c

b

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Figs. 5a–c
Virtual plan: frontal (a)
and sagittal views (b);
virtual stereolithographic
surgical template (c).

Figs. 5a & b

a

b
Fig. 5c

c

After orthodontic treatment, the patient underwent a preoperative cone beam computed tomography (CBCT; CRANEX 3Dx, SOREDEX, Tuusula,
Finland) scan, and diagnostic impressions were
taken using a polyether material (Impregum, 3M
ESPE, Seefeld, Germany) with a custom open tray
(Diatray Top, Dental Kontor, Stockelsdorf, Germany). Furthermore, model casts were poured in
Type IV stone (Techim Super Stone, Techim Group,
Milan, Italy) and a diagnostic wax-up was made.
The STL ﬁles derived from the scanned model and
wax-up were merged with the DICOM data
12 Volume 3 | Issue 1/2017

derived from the CBCT scan in the same virtual
implant planning software (NobelClinician, Nobel
Biocare, Kloten, Switzerland). Virtual planning
was completed by deﬁning a prosthetically driven
implant placement. Owing to the reduced space
between adjacent roots, a 3.0 mm implant was
planned (Osstem TSIII, Osstem, Seoul, South
Korea). After careful functional and esthetic evaluation and ﬁnal veriﬁcation, the approved virtual
plan was transmitted to a milling center (Nobel
Biocare) for the production of a stereolithographic
surgical template (Figs. 5a–c).

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Before implant placement, the stereolithographic surgical template was adapted to the
master cast. The patient underwent professional oral hygiene and received prophylactic
antiseptic (0.2% chlorhexidine for 1 min) and
antibiotic therapy (2 g of amoxicillin and clavulanic acid). Local anesthetic was administered
with a 4% articaine solution with epinephrine
1:100 000 (Ubistein, 3M ESPE). The surgical
template was placed intraorally in relation to
the opposing arch using the silicone surgical
index derived from the mounted casts and stabilized with two anchor pins. A ﬂapless guided
pilot drill was employed using the surgical template, and the continuity of the implant site was
evaluated with the aid of a periodontal probe
(PCPUNC156, Hu-Friedy, Milan, Italy). The implant was placed freehand in the planned anatomical site according to a one-stage approach,
without tissue grafting. The final insertion
torque was 37.5 N cm (iChiro Pro, Bien-Air
Dental, Biel, Switzerland).
A new deﬁnitive impression of the maxilla
was made using a polyether material (Impregum) and poured in Type IV stone (Techim
Super Stone). This master cast was
cross-mounted in a semi-adjustable articulator
and a temporary acrylic restoration was fabricated using a temporary titanium abutment
(Osstem). The temporary restoration was
screwed to the implant with prosthetic screws
tightened according to the manufacturer’s
instructions (30 N cm) 24 h after implant placement, as directed by an immediate loading
protocol. The prefabricated temporary acrylic
restoration was trimmed and polished chairside. A nonoccluding occlusal scheme was delivered (Fig. 6). After implant placement, the
patient received oral and written instructions
regarding medication, oral hygiene maintenance and diet. A periapical radiograph was
taken with the paralleling technique in order to
exclude radiolucency or other complications.
The ﬁnal restoration was delivered three
months after implant placement. The zirconia
framework was fabricated using CAD/CAM
technology (New Ancorvis, Bargellino, Italy)
and veneered with ceramic. The screw-retained
deﬁnitive restoration was ﬁnally attached at
the torque setting recommended by the manufacturer (30 N cm; Figs. 7 & 8). The occlusion
was carefully adjusted and the patient was
recalled every 4 months for hygiene maintenance and annually for occlusal adjustment
(Figs. 9 &10).

Discussion
In the present report, the case was treated
successfully with orthodontic space opening
and prosthetic replacement of the missing
lateral incisor with a single implant-supported
crown. This case report aimed to describe the
novel Osstem TSIII 3.0 mm (Osstem) implant
used, which allows for the replacement of
maxillary lateral incisors and mandibular incisors. Prompt diagnosis and an interdisciplinary approach, guided by functional and esthetic demands, are essential for the proper
management of such complex cases. Teenagers with late mixed dentition or newly developed permanent dentition often seek treatment for the congenital absence of maxillary
lateral incisors, because, during this period,
the esthetic problem becomes more evident.
When maxillary lateral incisors are missing, there are several factors to consider before treatment with space opening or closure.
These factors include the type of malocclusion, crowing/spacing, tooth size relationships, canine position, shape and color of the
canines, and upper lip length.6–8 The choice
between these two modalities of treatment
should not be made empirically. In most instances, the presence or absence of major
occlusal problems serves as the primary criterion for either space closure or space opening.9 Lateral incisal spaces should be closed in
cases in which malocclusions require the extraction of permanent mandibular teeth. 4
Mandibular extractions may be indicated to
relieve anterior or posterior arch length deficiency, to reduce mandibular dentoalveolar
protrusion or to compensate for a Class II
molar relationship. Some orthodontic patients
may be missing several permanent teeth, including maxillary lateral incisors. If teeth have
been missing for several years, the remaining
teeth may have drifted. In these patients,
ortho dontists and restorative dentists may
not know what the restorative requirements
are or what the eventual restorative treatment
plan should be. For these types of patients, it
is suggested to predetermine the final occlusal and restorative outcomes by creating diagnostic wax setups.10 In addition, the trial
setup will allow identification of tooth surfaces that require functional and esthetic reduction so that equilibration may be initiated
either at the beginning of or during the orthodontic treatment.

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Fig. 6

Fig. 6
Immediately loaded temporary
restoration.
Fig. 7
Deﬁnitive restoration.
Fig. 8
Periapical radiograph.
Fig. 9
Deﬁnitive restoration 1 year
after implant placement.
Fig. 10
Periapical radiograph 1 year
after implant placement.

Figs. 7 & 8

Figs. 9 & 10

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The diagnosis and treatment of growing children
with missing lateral incisors can be a problem
for many clinicians. If the patient and his or her
parents plan on him or her undergoing implant
treatment in the future, it is important that the
majority of vertical facial growth and tooth eruption be completed before implant placement.7
After completion of growth in body height, sequential cephalometric or hand–wrist radiographs verify the cessation of facial growth over
a time frame of approximately six months to one
year. The sequence of treatment in cases of
agenesis of anterior teeth must be carefully explained to both the patient and his or her parents.
They must realize that the orthodontic treatment is the beginning of the process, which is
to be followed by the scheduling of periodontal
therapy and ﬁnal restorations. It is crucial that
all of the treatment options be discussed with
the interdisciplinary team, just as all of the
options are explained in the orthodontic treatment phase.
Space closure is recommended for missing
lateral incisors in subjects with long faces, as it
is the preferred treatment for preserving arch
anchorage and avoiding clockwise rotation of
the lower jaw. In addition, it is the treatment of
choice in subjects with bimaxillary dental protrusion in order to avoid worsening of the proﬁle
or in cases of early treatment in adolescents.
Space closure can also be considered with two
types of malocclusions: a mandibular anterior
with severe dental crowding and a Class I malocclusion, for which the ﬁrst premolars and
canines are extracted to achieve mesialization
(thus obtaining a molar and canine Class I), as
well as a Class II malocclusion without crowding
and mandibular protrusion. Furthermore, space
closure may beneﬁt patients with a speciﬁc anterior relationship, speciﬁcally those with an
increased overjet and reduced overbite. Lastly,
the presence of third molars is an additional
factor that would be supported by space closure
mechanics. The color of the natural canine
should be approximately that of the central incisor. It is not uncommon for the canine to be
more saturated with color, resulting in a tooth
that is one to two shades darker than the central
incisor.
Space opening (between the canine and central incisor) is the second therapeutic option in
the treatment of missing lateral incisors. Space
opening and prosthodontic intervention are indicated in low-angle subjects and those with
retruded proﬁles in order to improve the labial

sagittal relationship. It is also the treatment of
choice in patients with molar Class I or III tendency in order to preserve an ideal occlusal anterior and posterior relationship. Space opening
is also of beneﬁt in cases with a reduced overjet
and increased overbite. As mentioned previously,
an important factor that clinicians should consider when deciding on treatment is the patient’s
age. Space opening is not recommended before
the age of 13 years in order to prevent the relapse
and progression of bone atrophy.11 In the case of
unilateral tooth agenesis, space opening is often
recommended in order to improve the esthetics
and preserve smile symmetry.12
According to Magne and Belser, there are
various subjective and objective criteria for the
assessment of an ideal smile.13 The midline is an
imaginary line located at the center of the face,
perpendicular to the interpupillary line. In a totally symmetrical face, the dental midline and
the facial midline should coincide, but this is
often not the case.14 According to Spear et al.,
a midline deviation greater than 4 mm can be
detected by the general public,15 whereas a midline deviation of 2 mm remains undetectable by
laypersons.14
Given these considerations, the choice of
opening space for the implant in our patient was
especially inﬂuenced by the presence of microdontia of the maxillary left lateral incisor and the
midline deviation of over 3 mm.
When examining the esthetics of the anterior teeth and overall smile, the clinician should
be aware of the morphology of the gingival contours, tooth contacts, tooth morphology and
tooth size problems. In order to obtain ideal esthetic results, worn incisal edges, tooth shape,
incisal contact, the contours of the gingival margins, and black triangles should be considered
before starting orthodontic treatment. The decision to reshape or add tooth structure should
be evaluated in light of the width-to-length
ratios of the golden proportion.16 It appears clinically that long, tapered triangular maxillary incisors have thin, arched gingival tissue with a
longer, delicate papilla and thin bone with a
smaller incisal contact point. In contrast, rectangular-shaped incisors tend to have thicker
gingiva with a ﬂatter, wider free gingival margin.
Furthermore, these latter teeth have broad contacts. Generally speaking, the more rectangular
the teeth, the thicker the alveolus and the
gingiva that house them.17
Present-day demands and expectations of
esthetic dentistry are growing. In order to pro-

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Implant and orthodontic treatment

vide esthetic anterior tooth shape and correct
agenesis, patients must be informed of their
total dental needs, not just those associated with
a limited specialty. In order to integrate and coordinate treatment, patients need to be offered
a total treatment approach that maximizes function, esthetics and oral health. In many common
dental malocclusions, orthodontic treatment
alone may not be enough.18
Computer-assisted, template-based implant
placement may help clinicians to perform successful implant therapy, avoiding elevation of
large ﬂaps or even eliminating ﬂaps completely
and thereby causing less pain and discomfort to
patients, particularly in complex cases.19–22 Correct estimation of the bone condition and the
implant position and precise drilling into the
bone according to the preoperative planning
may be essential in ensuring the successful
placement of an implant.

Conclusion
Comprehensive interdisciplinary rehabilitation
according to the CRANIO philosophy was effective in successfully restoring function and esthetics in a young female patient affected by
congenitally missing maxillary lateral incisor.

Competing interests
The ﬁrst author (MT) is the Research and Scientiﬁc Project Manager at Osstem AIC, Italy. Osstem, Seoul, South Korea, the manufacturer of
the implant system evaluated in this investigation, kindly donated the implant placed.
However, the data remained that of the authors
and in no manner did the manufacturer interfere
with the conduct of the trial or the publication
of the results.

References
1.
Kiliaridis S, Sidira M, Kirmanidou Y,
Michalakis K. Treatment options for
congenitally missing lateral incisors.
→ Eur J Oral Implantol.
2016;9 Suppl 1:S5–24.

7.
Kokich VO Jr. Congenitally missing teeth:
orthodontic management in the adolescent
patient.
→ Am J Orthod Dentofacial Orthop.
2002 Jun;121(6):594–5.

13.
Magne P, Belser U. Bonded porcelain
restorations in the anterior dentition:
a biomimetic approach.
→ Chicago: Quintessence.
2002. 406 p.

19.
Tallarico M, Meloni SM, Canullo L,
Polizzi G. Guided surgery for
single-implant placement: a critical review.
→ J Oral Science Rehabilitation.
2016 Dec;2(4):8–14.

2.
Muller TP, Hill IN, Peterson AC, Blayney JR.
A survey of congenitally missing
permanent teeth.
→ J Am Dent Assoc.
1970 Jul;81(1):101–7.

8.
Robertsson S, Mohlin B. The congenital
missing upper lateral incisor. A
retrospective study of orthodontic space
closure versus restorative treatment.
→ Eur J Orthod.
2000 Dec;22(6):697–710.

14.
Pinho S, Ciriaco C, Faber J, Lenza MA.
Impact of dental asymmetries on
the perception of smile esthetics.
→ Am J Orthod Dentofacial Orthop.
2007 Dec;132(6):748–53.

20.
Tallarico M, Meloni SM, Canullo L, Caneva
M, Polizzi G. Five-year results of a
randomized controlled trial comparing
patients rehabilitated with immediately
loaded maxillary cross-arch ﬁxed dental
prosthesis supported by four or six
implants placed using guided surgery.
→ Clin Implant Dent Relat Res.
2016 Oct;18(5):965–72.
doi:10.1111/cid.12380. Epub 2015 Oct 7.

3.
Stamatiou J, Symons AL. Agenesis of
the permanent lateral incisor: distribution,
number and sites.
→ J Clin Pediatr Dent.
1991 Summer;15(4):244–6.

9.
Zachrisson BU. Improving orthodontic
results in cases with maxillary incisors
missing.
→ Am J Orthod.
1978 Mar;73(3):274–89.

4.
Andrade DC, Loureiro CA, Araújo VE,
Riera R, Atallah AN. Treatment for agenesis
of maxillary lateral incisors: a systematic
review.
→ Orthod Craniofac Res.
2013 Aug;16(3):129–36.
5.
Silveira GS, Mucha JN. Agenesis of
maxillary lateral incisors: treatment
involves much more than just canine
guidance.
→ Open Dent J.
2016 Feb;10:19–27.

10.
Kokich VG, Spear FM. Guidelines of
managing the orthodontic-restorative
patient.
→ Semin Orthod.
1997 Mar;3(1):3–20.
11.
Beyer A, Tausche E, Boening K, Harzer W.
Orthodontic space opening in patients
with congenitally missing lateral incisors.
→ Angle Orthod.
2007 May;77(3):404–9.

6.
Thordarson A, Zachrisson BU, Mjor IA.
Remodeling of canines to the shape of lateral incisors by grinding: a long-term clinical
and radiographic evaluation.
→ Am J Orthod Dentofacial Orthop.
1991 Aug;100(2):123–32.

12.
Rosa M, Zachrisson BU. The space-closure
alternative for missing maxillary lateral
incisors: an update.
→ J Clin Orthod.
2010 Sep;44(9):540–9; quiz 561.

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15.
Spear FM, Kokich VG, Mathews DP.
Interdisciplinary management
of anterior dental aesthetics.
→ J Am Dent Assoc.
2006 Feb;137(2):160–9.
16.
Ricketts RM. The biologic signiﬁcance of
the divine proportion and Fibonacci series.
→ Am J Orthod.
1982 May;81(5):351–70.
17.
Morley J, Eubank J. Macroesthetic
elements of smile design.
→ J Am Dent Assoc.
2001 Jan;132(1):39–45.
18.
Kavadia S, Papadiochou S, Papadiochos I,
Zaﬁriadis L. Agenesis of maxillary
lateral incisors: a global overview of
the clinical problem.
→ Orthodontics (Chic.).
2011 Winter;12(4):296–317.

Journal of
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21.
Pozzi A, Tallarico M, Marchetti M, Scarfo B,
Esposito M. Computer-guided versus
free-hand placement of immediately
loaded dental implants: 1-year post-loading results of a multicentre randomised
controlled trial.
→ Eur J Oral Implantol.
2014 Autumn;7(3):229–42.
22.
Pozzi A, Tallarico M, Mangani F, Barlattani
A. Different implant impression techniques
for edentulous patients treated with CAD/
CAM complete-arch prostheses: a
randomised controlled trial reporting data
at 3 year post-loading.
→ Eur J Oral Implantol.
2013 Winter;6(4):325–40.

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Biomaterials for onlay bone grafts

Biological and physical properties
of bone block grafting biomaterials
for alveolar ridge augmentation
Abstract
Objective
Alberto Monjea & Hom-Lay Wanga
a

Graduate Periodontics, Department of Periodontics
and Oral Medicine, School of Dentistry, University of
Michigan, Ann Arbor, Mich., U.S.

Corresponding author:
Dr. Alberto Monje and Prof. Hom-Lay Wang
Department of Periodontics and Oral Medicine
School of Dentistry
University of Michigan
1011 North University Ave.
Ann Arbor, MI 48109-1078
U.S.
T +1 734 763 3383
amonjec@umich.edu
homlay@umich.edu
How to cite this article:
Monje A, Wang HL. Biological and physical properties of
bone block substitute biomaterials for ridge augmentation.
J Oral Science Rehabilitation.
2017 Mar;3(1):18–30.

Bone resorption of maxillary ridges is an unavoidable process that occurs
after tooth extraction. Many treatment alternatives have been proposed
to facilitate implant placement in these scenarios. Drawbacks such as
morbidity, cost and excessive resorption owing to the procedure have
prompted clinicians to seek biomaterials as an alternative to autogenous
bone. The objective of this article was to review the current state of the
art by means of the biological and physical properties of biomaterials used
for block grafting in atrophic maxillary ridges. Secondly, it was aimed
herein at presenting the clinical and histological ﬁndings when using these
biomaterials.
Materials and methods

An electronic and manual literature search was conducted by two independent reviewers using several databases, including MEDLINE, EMBASE,
Cochrane Central Register of Controlled Trials and Cochrane Oral Health
Group Trials Register databases, for articles written in English up to June
2016. Owing to the heterogeneity of the ﬁndings, quantitative assessment
could not be conducted. As such, a narrative review was carried out on the
biological and physical aspects of biomaterials used for block grafting.
Results

Both allogeneic and xenogeneic block grafts have been developed to overcome deﬁciencies of autogenous grafts. Allogeneic block grafts have been
widely investigated, but there is a lack of long-term follow-up. On the
contrary, xenogeneic block grafts have only limited scientiﬁc evidence of
their suitability for ridge reconstruction.
Conclusion

Allogeneic and xenogeneic bone block grafts represent a promising alternative to autogenous bone for ridge augmentation. Nonetheless, the evidence supporting xenogeneic block graft usage remains minimal; hence,
more long-term human studies are needed to validate their effectiveness.
In addition, using prefabricated scaffolds impregnated with growth factors
provides an interesting ﬁeld to be further explored.
Keywords

Bone grafting, bone biomaterials, allogeneic, xenogeneic, bone substitutes.
18 Volume 3 | Issue 1/2017

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Biomaterials for onlay bone grafts

Introduction
After tooth extraction, bone remodeling that
leads to bone resorption is a common phenomenon. Ridge resorption has made grafting procedures popular in implant and restorative therapy.1–4 These procedures aim at restoring width
and height for proper 3-D implant placement.
Numerous treatment alternatives have been
proposed (e.g., distraction osteogenesis and
guided bone regeneration with particulated
bone materials).5 Nonetheless, for extensive or
severely atrophic ridges, block grafting has been
advocated to be the most predictable approach.6, 7
Autogenous bone has been regarded as the
gold standard for bone reconstruction.8 This can
be harvested from different locations based
upon the extension of the atrophic area.8 While
intraoral bone block grafts (mandibular ramus
or mental symphysis) can be harvested with a
less traumatic approach, the amount is often
limited. However, extraoral bone block grafts
(calvaria or iliac crest) fulﬁll the requirements
in terms of quantity, but they increase the cost
and lead to some sequelae for the donor site.
Regardless of the harvesting location, autogenous block grafts might be further classiﬁed
depending on their origin. For example, intramembranous grafts (mandibular ramus and
calvaria bone) have less bone resorption and the
process of bone remodeling or “creeping substitution” takes longer9 compared with endochondral bone (iliac crest).10 Hence, it is important to take this into consideration when planning
implant treatment so that it will not cause extensive bone remodeling that threatens the ﬁnal
adequate prosthetically driven implant position.11, 12
Indeed, autologous bone has osteogenic capacity;8 in other words, bone can potentially
grow in between the interface of the graft and
the host bone. Nevertheless, as already mentioned, the drawbacks associated with this approach have encouraged clinicians to use alternatives, such as allogeneic or xenogeneic bone
blocks.13, 14 These treatment modalities not only
reduce the possibility of experiencing morbidity, but also shorten the treatment and, hence,
increase patient acceptance and satisfaction.
The mechanism of forming new mineralized
tissue is mediated by the mesenchymal cells,
which differentiate into osteoblasts that are
coordinated by glycoproteins (bone morphogenetic proteins).15 Hence, after an inﬂammatory

process that ends in gradual substitution, the
newly formed bone is obtained,16 or in this case
hard tissue capable of obtaining ﬁrst implant
stability and subsequently osseointegration.
In general, allogeneic and xenogeneic block
grafts do not contain osteoprogenitor cells and,
consequently, integration with the native bone
might be arduous. Promising results have been
shown in the literature with application of these
block grafts for bone regeneration.17, 18 Depending on their origin, they can be either from
human (cadaver), known also as allografts, or
from animal origin (equine and bovine), which
are also called xenografts. Once harvested, the
grafts must be preserved, and each manufacturing company has developed its own process
that can potentially determine the properties of
the respective biomaterial.
The objective of this article was to review
the biological and physical properties of block
grafting biomaterials available for bone regeneration in atrophic maxillary ridges. Furthermore, the aim was to present the human and
animal clinical and histological ﬁndings of biomaterials used for maxillary reconstructions.

Materials and methods
Information sources

An electronic literature search was conducted
by two independent reviewers (AM and HLW)
of several databases, including MEDLINE, EMBASE, Cochrane Central Register of Controlled
Trials and Cochrane Oral Health Group Trials
Register databases, for articles written in
English up to June 2016.
Screening process

Combinations of controlled terms (MeSH and
EMTREE) and keywords were used whenever
possible:
(((((((Alveolar bone atrophy[MeSH Terms])
OR alveolar bone loss[MeSH Terms])
AND bone grafting[MeSH Terms])
OR allograft[MeSH Terms])
OR xenograft[MeSH Terms])
OR biomaterials[MeSH Terms])
AND block)
OR onlay
OR

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Biomaterials for onlay bone grafts

(((((((("alveolar bone loss"[MeSH Terms]
OR "alveolar bone loss"[MeSH Terms])
AND bone graft[Title/Abstract])
AND block[Title/Abstract])
OR onlay[Title/Abstract])
AND biomaterial[Title/Abstract])
OR allogeneic[Title/Abstract])
OR allograft[Title/Abstract])
OR xenogeneic[Title/Abstract])
OR xenograft[Title/Abstract]
AND "humans"[MeSH Terms]

– The trabeculae-like structures that form the
scaffold must leave enough space for the formation of new vessels by the endothelial cells
that will supply of all the nutrients and osseous
cells to the scaffold.
Therefore, as occurs in autogenous bone
blocks, biomaterials undergo three steps:
(1) colonization of host cells; (2) degradation
of the biomaterial while turnover is occurring;
and (3) maturation of the newly formed bone
and integration with the recipient site’s bone
(Fig. 1).
However, biomaterials in bone grafting must
fulﬁll other properties besides biological ones.
This will allow the material to interact with the
host environment and, thus, increase the possibility of bone formation and long-term stability.
These properties should include:

Additionally, a manual search of periodonticsand implantology-related journals, including the
Journal of Dental Research, Journal of Clinical
Periodontology, Journal of Periodontology, and
International Journal of Periodontics and Restorative Dentistry, from January 2015 up to June
2016, was performed to ensure a thorough
screening process. Furthermore, references of
included articles were screened to check all – Mechanical properties: Among these properties are resistance, resilience, stiffness, fragilavailable articles.
ity, tenacity, ductility and malleability. The
Biomaterials’ properties
result of the combination of these mechanical
properties will determine the handling of the
“Biomaterial” refers, generally speaking, to mamaterial more than its capacity as scaffold for
terial that has been developed to interact with
bone regeneration.21 However, it is important
the biological system, acting as a scaffold for
to note that, generally, the stiffer the biomareplacement and repair of, in this case, lost bone.
terial is, the longer it lasts due to the more
rigid element.
Firstly, a biomaterial must be biocompatible,
which is deﬁned as the capacity that the materi- – Surface phenomena: It is important to take
into consideration the internal energy, surface
al has to elicit an appropriate biological response
and, thus, not be detected as a foreign body by
tension, wettability, and adhesion and cohethe host. In addition, it must have sufficient dusion of the biomaterial to be used for bone
rability to carry out the task for which it was deregeneration. These properties are in part
veloped. Further, it must be chemically stable
responsible for the aggregation and attachment of vital osteogenic cells in a nonvital
(neither toxic nor carcinogenic for the host).
For block grafts used in regeneration, an
structure (scaffold).21
ideal biomaterial, from the cellular and mo - – Physical properties: Three main properties are
lecular standpoint, must have the following
included within this group:
properties:
– Thermals: thermal expansion, thermal con– Its design enables osteogenic cells to reach the
traction, thermal insulation, melting point
entire block by osteoconduction and osteoinand interval;
duction in order to complete the turnover pro– Electrics: electric conductivity, electrical
cess. In order to permit osteoblastic growth and
resistivity and oral galvanism; and
mineralized tissue production, the ideal size of
– Optics: color and appearance.
19
the micropores should be within 180–600 μ.
This is of crucial importance inasmuch as os- – Chemical properties: toxicity, chemical stabilteoblasts (15–50 μ) and stem cells (5–12 μ) have
ity, half-life, ﬂammability or enthalpy of for20
to proliferate guided through the pores. The
mation among others.
biomaterial itself must be replaced by vital bone – Rheological properties: apparent viscosity,
(newly formed bone). Therefore, the biomatenormal force coefficients, storage modulus,
complex viscosity and complex functions of
rial’s degradation must be in accordance with
nonlinear viscoelasticity.
the remodeling process.
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Biomaterials for onlay bone grafts

Fig. 1

Fig. 3
Periapical radiograph showing
the orthodontic miniscrew.
Figs. 4a–c
Orthodontic treatment:
right (a), left (b)
and occlusal (c) view.

Va s c u l a r i z a t i o n

Biomaterials used in bone regeneration lack
cells, proteins and vessels. In this manner, risk
of disease transmission is minimized. Therefore,
cells from the recipient site of the graft carry
out the process of neoangiogenesis, an essential
step for successful bone regeneration.22 Neovascularization indeed is fundamental because
it supplies the avascular scaffold with oxygen
and the nutrients required for cell growth and
differentiation. 23 Accordingly, newly formed
bone and resorption of the block graft rely upon
the neoangiogenesis process. Numerous growth
factors, such as vascular endothelial growth
factor (VEGF), ﬁbroblast growth factor (FGF),
some subgroups of the transforming growth
factor beta family (TGF-ʹ), transcription factor
to induce hypoxia (HIF), angiopoietin (Ang-1),
hepatocyte growth factor (HGF), plateletderived growth factor (PDGF-BB), insulin-like
derived growth factor (IGF-1, IGF-2) and neurotrophic growth factor (NGF) are involved in the
process.24 Accordingly, VEGFs and their receptors are in charge of the molecular and cellular
cascade inasmuch as they lead the development
of the endothelial system by vasculogenesis,
angiogenesis and the lymphatic net. Additionally, VEGFs play a meaningful role in skeletal
growth and in bone repair and regeneration.25
Likewise, FGFs are in charge of promoting proliferation and differentiation of endothelial cells
and ﬁbroblasts. On the contrary, TGFs increase

extracellular matrix development. HIFs mediate
the effects of hypoxia on the cells. Ang-1 stabilizes the vessels. However, HGFs act on epithelial and endothelial cells for organ regeneration
and wound healing. Commonly used as exogenous growth factors in bone regeneration, the
PDGF family plays an important role in angiogenesis. IGFs in contrast have endocrine effects
upon the host. Lastly, NGFs, also known as neurotrophins, maintain nerve cells within the horizontal newly formed bone.26, 27
In bone regeneration using block grafts as
scaffolds, new tendencies are arising, since, contrary to autogenous grafts, early neoangiogenesis is essential for biomaterial survival and integration. In consequence, techniques such as
the delivery of stem cells and growth factors in
order to accelerate the process have been closely examined recently with promising results.28
However, there is still a lack of results to make
any conclusive statement in this regard.
Types of block graft biomaterials

1. Allogeneic block grafts
The use of allografts represents a fair alternative
to autogenous block grafts, since the blocks are
harvested from the same species as that of the
recipient. The ﬁrst bone allografts were performed in late 19th century by a group of surgeons who reconstructed an infected humerus
with a graft harvested from the tibia of the same

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Fig. 1
Descriptive illustration of the
onlay bone grafting procedure.
In order to be successful,
the three elements must be
achieved to ensure a proper
creeping substitution process.

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Biomaterials for onlay bone grafts

patient.29 The establishment of the U.S. Navy
Tissue Bank in 1990 was a signiﬁcant inﬂuencing factor for the wide use of bone allografts.
The use of allografts has continued to increase
since then.30
Properties
The properties of allograft material are directly
related to its processing and its precedence.31
Allogeneic block grafts may be prepared as
fresh, frozen and freeze-dried. Nowadays, the
vast majority of grafts are carefully screened,
harvested, processed and distributed, and this
is governed by the American Association of Tissue Banks. The risk of disease transmission is
often minimized through the above processes.32, 33 In addition, during graft preparation, the
antigenic components are carefully removed to
eliminate any potential host immune response.32
Fresh or frozen allografts retain both osteoinductive and osteoconductive capacities, allowing a slightly faster bone turnover than that of
freeze-dried allografts. However, the risks of
disease transmission and host reactions are
slightly increased,34 whereas the immune response is reduced in freeze-dried allografts.34
This is due to the elimination of the cells by embedding the graft in antibiotic wash twice for 1 h
and then storing it at -70 °C to dry up to 5% of
the water.35, 36 Another issue to bear in mind is
that, because of the drying, mechanical properties are weakened. Hence, microfracture of the
grafts might easily occur. Consequently, for this
type of block allograft, rehydration is suggested
prior to placement in order to regain some of the
mechanical properties. 37 Currently, Zimmer
Biomet Dental (Carlsbad, Calif., U.S.) has patented its suitable preparation sequence (Fig. 2).
This is the Tutoplast process, which includes
cleaning and ultrasonic lipidization in acetone,
an osmotic and later oxidative treatment, ending
with dehydration in sequential acetone baths
and gamma irradiation.38 The result of this process is a greater preservation of the minerals
and collagen matrix, leading to rapid bone turnover.39
Clinical outcomes
Bone block allografts are a relatively novel alternative to autogenous grafts for horizontal
and/or vertical bone augmentation of the atrophic maxilla (Table 1). In 1999, the ﬁrst case of
using an allogeneic block bone graft for bone
regeneration was reported. In that case, dental
implants for oral rehabilitation were successful22 Volume 3 | Issue 1/2017

ly placed three months after the grafting procedure.18 Since then, multiple prospective human
clinical trials have been published demonstrating proof of principle for this human allograft
block usage.40–56
From our clinical experience and others’,
when the human allograft is exposed to the oral
cavity, it often leads to graft failure.42, 57 Moreover, it has much higher failure rate in the mandible than in the maxilla owing to difficulty in
ﬂap advancement and a thinner soft-tissue biotype.58 Failure of a block graft generally occurs
in the early stages of graft healing.41, 45, 52, 55
In addition, bone graft resorption occurs during
healing, which is the same as with autogenous
grafts. However, greater bone loss occurs at six
months after placement compared with autogenous bone harvested from the mandibular ramus
(52.00 ± 25.87% vs. 25.00 ± 12.73%, respectively). 46 A recent systematic review found
promising results on the use of allogeneic bone
grafts for horizontal bone augmentation in maxillae.59 It was shown that not only high graft and
implant survival rates had been achieved (98.0%
and 96.9%, respectively), but also that a weighed
mean of 4.79 mm of horizontal bone had been
gained over a mean follow-up period of 23.9
months.
Histological and
histomorphometric outcomes
Indeed, allogeneic block grafts do not behave
like autogenous bone from the cellular standpoint because of the lack of osteogenic potential;
notwithstanding, respecting a proper healing
time (more than six months), this biomaterial
results in similar clinical healing to that of native
bone40–56 (Figs. 3a–c & 4). Acocella et al. showed
that, after nine months, a high number of empty
osteocyte lacunae were still present and that
more ﬁbrous tissue was present than in the samples taken previously. 40 Additionally, newly
formed bone (61.96 ± 11.77%) was surrounded
by nonvital bone with empty osteocyte lacunae.
At the same time after healing, Contar et al.
demonstrated a lamellar arrangement around
Haversian canals interspersed with osteocytes
in lacunae.43 They also observed that the central
portions of the grafts showed osteocytes with
a higher number of empty lacunae.
When histological results are compared
between groups (allogeneic vs. autogenous),
behavioral dissimilarities are displayed. Lumetti
et al. showed that, after six months of healing,
osteocyte lacunae were mostly empty for the

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Biomaterials for onlay bone grafts

Fig. 2
Scanning electron microscopy
image of the Puros Block
Allograft (Zimmer Biomet
Dental) microarchitecture
(75× magniﬁcation).
(Courtesy of Zimmer Dental).

Fig. 2

Figs. 3a–c
Histological samples of Puros
Block Allograft six months
after a regenerative procedure
of the atrophic maxillae
(100× magniﬁcation [a] and
400× magniﬁcation [b & c]).
Fig. 4
Histological sample of J-Block
Puros Allograft six months
after a regenerative procedure
for horizontal augmentation
in atrophic maxillae. Note the
high amount of newly formed
bone present, while the
percentage of remaining
material is decreased.

Figs. 3a–c

a
+ Newly-formed bone
% Non-mineralized tissue

b

c

) Remaining allogeneic grafting material
ٔOsteocyte lacunae

Fig. 4

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Biomaterials for onlay bone grafts

Author (year)

Study design

Groups

No. of
patients

No. of sites
grafted

Location of grafted sites

Bone augmentation (V/H)

Type of bone block graft

Acocella et al. (2012)40

Prospective case series

NCG

16

18

Anterior/posterior

H

Monocortical
fresh-frozen

Barone et al. (2009)41

Prospective case series

NCG

13

24

Anterior (13)/ posterior (9)

H (19)/V (5)

Corticocancellous
deep-frozen

Chaushu et al. (2010)42

Prospective case series

NCG

101

90

Anterior (58)/ posterior
(32)

NC

Cancellous fresh-frozen

Contar et al. (2009)44

Prospective case series

NCG

15

34

Anterior/posterior

H

Cancellous/cortical
fresh-frozen
Cancellous/cortical
fresh-frozen

Contar et al. (2011)43

Prospective case series

NCG

18

39

Anterior/posterior

NC
Cortical fresh-frozen

Wallace & Gellin (2010)56

Spin-Neto et al. (2013)

Prospective case series

NCG

12

16

AL

13

17

AT

13

17

Prospective case series

Anterior/posterior

Anterior (14)/posterior (3)

H

H

Cancellous fresh-frozen
Corticocancellous
deep-frozen
Mandibular ramus

Novell et al. (2012)52

Prospective case series

NCG

12

20

Anterior/posterior

H/H + V

Cortical/cancellous
fresh-frozen

Deluiz et al. (2013)45

Prospective case series

NCG

24

24

Anterior/posterior

H

Corticocancellous
fresh-frozen

Nissan et al. (2011)51

Prospective case series

NCG

20

28

Anterior

H (27)/V (12)

Cancellous fresh-frozen

Nissan et al. (2011)51

Prospective case series

NCG

31

46

Anterior

H (42)/V (27)

Cancellous fresh-frozen

50

Prospective case series

NCG

11

11

Anterior

H/V

Cancellous fresh-frozen

AL

12

12

Nissan et al. (2008)

Lumetti et al. (2012)46

Spin-Neto et al. (2013)55

Peleg et al. (2010)53

RCT

Anterior/posterior

H

AT

12

12

Mandibular ramus

AL

6

17

Cortical fresh-frozen

Prospective case series

Prospective case series

Corticocancellous
fresh-frozen

Anterior/posterior

AT

6

12

NCG

34

38

Mandibular ramus

Anterior (31)/ posterior (7)

RCT = randomized controlled trial; AL = allogeneic graft; AT = autogenous graft; H = horizontal; V = vertical; Y = yes; N = no; MCA =
mineralized cortical allograft;
BBM = bovine bone mineral; NC = not clear; NM = not mentioned; NCG = no control group.
Table 1

24 Volume 3 | Issue 1/2017

H

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Oral Science & Rehabilitation

H/H + V

Corticocancellous
fresh-frozen

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Biomaterials for onlay bone grafts

Membrane
(Y/N)

Additional grafting
material/growth factor

Healing
period
(months)

Histological
analysis
Resorption (%)
Newly formed
bone (%)

Characteristics

N

N

9

11.45 ± 8.37

61.96 ± 11.77

A high number of empty osteocyte
lacunae were still present and more
ﬁbrous tissue was present than in the
samples taken previously. Newly formed
bone was surrounded by nonvital bone
with empty osteocyte lacunae.

N

Cancellous allograft
particles

5

NM

NM

NM

Y

N

6

NM

NM

NM

N

N

NC

NM

NM

Mature and compact osseous tissue
surrounded by marrow spaces

N

N

9

NM

NM

Lamellar arrangement around Haversian
canals interspersed with osteocytes in
lacunae. No evidence of inﬂammatory
inﬁltrate. The central portions revealed
osteocytes with a higher number of
empty lacunae.

Y

MCA + rhPDGF-BB

5

NM

NM

NM

Y

N

6

NC

NM

NM

NM

NM

NM

NM

Y

8

13.02 ± 3.86

NM

Newly formed bone with osteocytes was
observed at all of the time points.
Osteocyte presence was higher at 4
months. Vessels were also detected
abundantly in the samples.

Freeze-dried allograft
particles
N

Y

Particulate BBM

6

NM

NM

NM

Y

Particulate BBM

6

10.00 ± 1.00

NM

NM

Y

Particulate BBM

6

NM

NM

NM

NC

Osteocyte lacunae were mostly empty.
Newly formed bone contained viable
osteocytes. Bone-forming osteoblasts
and ﬂuorescent labeling were detected.
Dense connective tissue with the
presence of inﬂammatory cells (WM
score = 1.67) and eroded areas.

NC

Osteocyte lacunae were mostly empty.
Newly formed bone contained viable
osteocytes. Bone-forming osteoblasts
and ﬂuorescent labeling were detected.
WM inﬂammatory score = 1.

NM

Large segments of necrotic bone with
empty osteocyte lacunae and little
osteoclastic activity. Blood vessels were
invading the Haversian canals of the
material. No direct contact was found
between remodeled and grafted bone.
Some osteoclastic activity surrounded by
connective tissue with no presence of
inﬂammatory cells by newly formed bone
failed to invade the graft.

NM

NM

Small areas of necrotic bone with
abundant presence of osteocytes. No
difference between the grafted and the
host bone.

NM

NM

NM

52.00 ± 25.87
Y

Particulate fresh-frozen

6

25.00 ± 12.73

NM
Y

Y

N

N

7

4

Journal of
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Volume 3 | Issue 1/2017 25

Table 1
Studies demonstrating the
clinical and histological
characteristics of the
prospective (cohort and case
series) testing of allograft
block grafts for horizontal
and /or vertical bone
augmentation of the atrophic
maxilla.

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Biomaterials for onlay bone grafts

allogeneic block graft group46 and that newly
formed bone contained viable osteocytes. In
these samples, bone-forming osteoblasts were
detected. Dense connective tissue with the presence of inﬂammatory cells and eroded areas
were also reported. Minimal differences were
shown for the autogenous block graft group, in
which no connective tissue was found and the
presence of inflammatory cells was low.
However, Spin-Neto et al. found major differences between groups.55 The following histological characteristics were found to be associated with allogeneic bone block grafts: (a) large
segments of necrotic bone with empty osteocyte
lacunae and little osteoclastic activity; (b) blood
vessels invading the Haversian canals of the
material—no direct contact was found between
remodeled and grafted bone; and (c) some osteoclastic activity surrounded by connective
tissue with no presence of inﬂammatory cells
by newly formed bone failed to invade the graft.
On the contrary, autogenous block grafts presented small areas of necrotic bone with a higher
number of osteocytes and a smoother junction
between the graft and host bed. Therefore, from
the cellular standpoint, allogeneic block grafts
in the early stages of healing behave in a different manner to autogenous block grafts.
However, the long-term outcome and differences remain to be determined.
2. Xenogeneic block grafts
Xenografts, which are derived from a genetically different species than the host, represent
another potential alternative to autogenous
block grafts for bone augmentation. Similar to
human allografts, the lack of osteogenic capacity makes them less predictable in terms of graft
incorporation into host bone. In addition, lack of
human cells turns xenografts into scaffolds with
no osteoinductive potential. Despite its novel
applicability as block grafts for augmenting severely atrophied bone, this type of biomaterial
has been widely used as particulate bone graft,
showing excellent outcomes by means of space
maintenance.60–62 Thus far, there is a scarcity of
literature regarding this biomaterial for onlay
grafts, and xenogeneic block grafts have been
used more commonly as inlay grafts. As mentioned above, vascularity for this biomaterial is
even more critical for success and, consequently, a three-wall defect (as displayed by host bone
for inlay grafts) often makes this approach more
reliable. However, an advantage of using xeno26 Volume 3 | Issue 1/2017

geneic biomaterial is that, owing to its slow rate
of resorption, space is better maintained over
the long term (Fig. 5).63, 64
Currently, two types of xenografts are available as blocks for bone augmentation: bovine
and equine. While deproteinized bovine bone
relies on its acceptability by clinicians, equine
bone has shown to be less fragile to fracture.65
However, as mentioned, more studies are needed to verify the viability of this type of biomaterial in comparison to autogenous or allogeneic
block grafts.
Properties
In contrast to human-derived bone, xenogeneic
grafts do not have osteoinductive potential.
Therefore, they are used only as scaffolds for
space maintenance and cell migration guidance.
Geistlich Bio-Oss (Geistlich Pharma, Wolhusen,
Switzerland), a bovine-derived biomaterial, is
the most widely used xenogeneic graft. This
biomaterial is claimed to have all organic material removed, so is nonantigenic. A modiﬁed
Geistlich Bio-Oss block that contains more collagen components for improving its manageability has also been introduced.66 Equine bone
blocks have recently been introduced and have
shown to provide an improved scaffold for cases
of severe atrophy owing to this bone’s natural
trabecular structure.67
Xenogeneic biomaterials, albeit not posing
osteoinductive potential, are claimed to serve
as slow-resorption scaffolds capable of promoting bone formation.68, 69 Nonetheless, more
studies on this material are still needed to better
understand its overall properties and long-term
results.
Clinical outcomes
As mentioned before, studies on xenogeneic
block grafts are limited.8 At this point, only a few
in vivo studies have been carried out on this biomaterial.66, 67, 70–72 The xenogeneic block graft has
been advocated for bone augmentation. Steigmann presented the ﬁrst human case report that
used this biomaterial for horizontal bone augmentation in the maxillary anterior region.85 Li
et al. successfully used Geistlich Bio-Oss blocks
for horizontal bone augmentation via a subperiosteal tunneling approach.70 This might represent an alternative approach for placing this
speciﬁc biomaterial owing to the success rate it
achieved. Despite these preliminary results, we
still need more evidence to support the use of
xenogeneic materials for onlay block grafting.

Journal of
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Biomaterials for onlay bone grafts

Fig. 5

Regarding xenogeneic graft resorption, Araújo et
al. in a dog study showed that the Geistlich
Bio-Oss block graft is capable of retaining its dimension with moderate amounts of new bone
formed at the base of the graft, while autogenous
block grafts undergo 30% and 50% graft resorption.71 Likewise, De Santis et al. demonstrated
superior volumetric stability of deproteinized
bovine bone mineral compared with autogenous
block grafts harvested from the mandibular
ramus in a dog study (0.2 mm vs. 0.9 mm of horizontal resorption, respectively).73
Histological and
histomorphometric outcomes
Animal studies have shown that both bovine
Geistlich Bio-Oss and equine eHac (Geistlich
Pharma) blocks demonstrated similar histological results. In the early stages of healing, the
grafts were surrounded by ﬁbrovascular connective tissue with no signs of necrosis, osteolysis or tissue degeneration.66 In contrast,
Schwarz et al. showed that, after 12 weeks of
healing, bovine bone had no signs of degradation, while equine bone presented with an increase in osteoclasts and multinucleate giant

cells.67 Additionally, it was shown that the
amount and extent of bone ingrowth was
higher for equine bone blocks, although this was
not of statistical signiﬁcance. Moreover, Araújo
et al. evidenced the lesser osteogenic capacity
of xenogeneic blocks, compared with autogenous grafts, by means of mineralized tissue
(47.5 ± 5.0% vs. 23.3 ± 3.0%, respectively).17
Similarly, ﬁndings by De Santis et al. illustrated
the poor incorporation of the block graft into the
pristine bone for horizontal ridge augmentation,
demonstrating that, while 77% of the autogenous bone presented with vital mineralization,
only 5.9% of the deproteinized bovine bone
could be identiﬁed as new bone formation.73
Therefore, it depends upon the clinician’s judgment regarding whether it is preferable to maintain the space or improve predictability by ensuring faster bone turnover.
Future directions

In order to facilitate bone graft adaptation, speed
up the surgical procedure and limit any potential
graft mobility or dead space, prefabrication of
graft scaffolds using advanced computed

Journal of
Oral Science & Rehabilitation

Volume 3 | Issue 1/2017 27

Fig. 5
Scanning electron microscopy
image of pore morphology
of cancellous bovine bone
(50× magniﬁcation) by
Dr. Michael Buﬂer. (Courtesy
of Geistlich Pharma, 2014)

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Biomaterials for onlay bone grafts

tomography is the next wave of bone regeneration and repair.74, 75 The idea of these scaffolds
for bone regeneration is based upon their ability
not only to maintain space, but also to create a
3-D graft structure that mimics the body’s own
extracellular matrix into which cells attach, migrate and proliferate.76, 77 The porosity in such a
scaffold biomaterial is important because it
allows the transport of nutrients and facilitates
tissue ingrowth. Hollister et al. proposed that
the ideal scaffold should possess the following
four properties: form, function, ﬁxation and formation.74 Wagoner Johnson and Herschler further pointed out that scaffolds should possess
biocompatibility, conductivity, bioactivity,
osteoinductive and interconnected porosity.78
Hence, synthetic scaffolds are currently being
studied in animal models and in vitro.79–84 The
application of gene therapy (mesenchymal stem
cells or human-derived growth factors) via prefabricated scaffolds is the focus of much research at present because growth factors can
be used to accelerate the wound-healing process
and to promote mesenchymal stem cell migration and maturation.

evidence supporting the use of xenogeneic block
grafts remains minimal; hence, more long-term
human studies are needed to validate their
effectiveness. In addition, using prefabricated
scaffolds impregnated with growth factors provides an interesting ﬁeld to be further explored.

Competing interests
The authors do not have any ﬁnancial interests,
either directly or indirectly, in the products or
information listed in the paper.

Acknowledgments

This paper was partially supported by the
University of Michigan’s Periodontal Graduate
Student Research Fund. In addition, we would
like to thank Mr. Hai Bo Wen (Director of
Research, Zimmer Biomet Dental), Ms. Vanesa
Álvaro (Scientiﬁc Marketing Manager, Inibsal
Dental) and Dr. Varvara Mitropoulos (Project
Manager Clinical Science, Geistlich Pharma) for
providing the scanning electron microscopy images. Lastly, we would like to thank Dr.
Conclusion
Francisco O’Valle (Department of Pathology,
School of Medicine and Institute of BiopatholoAllogeneic and xenogeneic bone block grafts gy and Regenerative Medicine, University of
represent promising alternatives to autogenous Granada, Granada, Spain) for the histological
bone for ridge augmentation. Nonetheless, the analysis shown in Figure 4.

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Felice P, Marchetti C, Iezzi G, Piattelli A, Worthington H,
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Felice P, Piana L, Checchi L, Corvino V, Nannmark U,
Piattelli M. Vertical ridge augmentation of an
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Fontana F, Rocchietta I, Dellavia C, Nevins M, Simion M.
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Schwarz F, Ferrari D, Balic E, Buser D, Becker J, Sager M.
Lateral ridge augmentation using equine- and
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study in dogs.
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2010 Sep;21(9):904–12.
Epub 2010 May 9.
68.
Botticelli D, Berglundh T, Lindhe J. The inﬂuence of a
biomaterial on the closure of a marginal hard tissue defect
adjacent to implants. An experimental study in the dog.
→ Clin Oral Implants Res.
2004 Jun;15(3):285–92.
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Carmagnola D, Adriaens P, Berglundh T. Healing
of human extraction sockets ﬁlled with Bio-Oss.
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Steigmann M. A bovine-bone mineral block for
the treatment of severe ridge deﬁciencies in the anterior
region: a clinical case report.
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Botticelli D. Healing at mandibular block-grafted sites. An
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Wagoner Johnson AJ, Herschler BA.
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Rosa V. What and where are the stem cells for dentistry?
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Iwata T, Yamato M, Ishikawa I, Ando T, Okano T. Tissue
engineering in periodontal tissue.
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calvarial defects in rabbits with platelet-rich plasma as
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with mesenchymal stem cells on vertical bone
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83.
Kim S, Jung UW, Lee YK, Choi SH. Effects of biphasic
calcium phosphate bone substitute on circumferential
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[32] => JOSR_A4_Editorial_03.qxp_Layout 1

Guided bone regeneration in periimplantitis therapy

Retrospective analysis
of periimplantitis therapy
of 158 implants

Abstract
Objective
Jörg-Ulf Wiegner,a Hermann Klinsmanna
& Toralf Kömmlingb
a
b

Private practice, Saalfeld, Germany
Private practice, Gera, Germany

The objective of the retrospective analysis was to evaluate the efficacy of
periimplantitis treatment up to a ﬁve-year observation period.
Materials and methods

Corresponding author:
Dr. Jörg-Ulf Wiegner
Saalstraße 35
07318 Saalfeld
Germany
T: +49 3671 460933
wiegner@saalepraxis.de

Patients treated for periimplantitis between 2009 and 2015 were included. Before therapy, the patients underwent professional tooth cleaning,
defect class diagnosis and thorough mechanical cleaning of the implant
surface. In the case of intraosseous defects, a deproteinized bovine bone
mineral and a native bilayer collagen membrane were used according to
the concept of guided bone regeneration. Retrospectively, plaque index,
full-mouth bleeding on probing and probing pocket depth were analyzed
before the therapy and at recall visits up to 56 months after therapy.

How to cite this article:
Results
Wiegner JU, Klinsmann H, Kömmling T.
Retrospective analysis of periimplantitis therapy
of 158 implants.
J Oral Science Rehabilitation.
2017 Mar;3(1):32–42.

Out of 22,724 implants, 107 patients with 158 implants underwent periimplantitis therapy and these had been in place for nine months to 15 years.
Fifteen implants (9.49%) had to be extracted despite therapy. Most of the
periimplantitis infections had occurred within ﬁve years after implantation
(108 implants; 68.4%). In 45 implants (28.5%), therapy had included
guided bone regeneration. Before therapy, bleeding on probing was 100%.
Bleeding on probing was absent in 50.0% of implants at 12 months and
in 73.1% of implants examined 49–56 months post-therapy. Probing
pocket depth was reduced from 4.92 ± 1.93 mm before therapy to
2.67 ± 0.88 mm after 12 months and remained stable up to 56 months
post-therapy (2.71 ± 0.30 mm).
Conclusion

Using a treatment approach including a presurgical hygiene phase and
considering the defect morphology, periimplantitis therapy was mostly
successful in terms of implant survival (90.5%).
Keywords

Periimplantitis, oral hygiene, defect class, guided bone regeneration.

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Guided bone regeneration in periimplantitis therapy

Introduction
Implant therapy is a well-established method to
restore missing teeth. However, periimplant tissue infections due to bioﬁlm formation may
compromise implant survival. The term “periimplantitis” describes an inﬂammatory process in
the periimplant mucosa with additional signs of
bone loss.1 Periimplantitis occurs in around 10%
of implants and 20% of patients.1–3 A very recent
meta-analysis reported a mean prevalence of
22% (CI: 14–30%) for periimplantitis.4
Risk factors for periimplantitis are poor plaque
control, history of periodontitis, smoking, uncontrolled diabetes, periimplant cement residue,
genetic factors, occlusal overload and history of
periimplantitis.5, 6 Current strategies for periimplantitis therapy include a pretreatment phase
with professional tooth cleaning, optimization of
plaque control with prosthesis adjustment if necessary and nonsurgical debridement.7–9 Afterward, in the surgical phase, a full-thickness ﬂap
is prepared and the contaminated implant surface
is thoroughly cleaned. Intraosseous defects can
be ﬁlled using a bone substitute or tissue graft
material with or without a resorbable membrane.
The postsurgical protocol includes systemic antibiotic therapy and chlorhexidine rinsing during
the healing phase, followed by the maintenance
phase with regular recall visits, ranging from
three to six months.
Regenerative surgical therapy has been
shown to predictably obtain partial to full defect
ﬁll,10 although the outcome may be inﬂuenced
by the defect morphology11 and implant surface.12 According to the concept of guided bone
regeneration (GBR), the use of a deproteinized
bovine bone mineral (DBBM) either with or without a native bilayer collagen membrane (NBCM)
has been evaluated in various clinical studies and
demonstrated marked short-term clinical improvements and promising long-term results.12–16
The aim of our retrospective evaluation was to
analyze the efficacy of the periimplantitis treatment with or without bone augmentation in
patients over a long-term observation period up
to ﬁve years post-therapy.

plants had been inserted between 1993 and
2014 by the same surgeon (JUW) according to
the manufacturers’ instructions. Implant systems included Steri-Oss (Nobel Biocare, Zurich,
Switzerland), CAMLOG implant system (Cylinder Line, Screw Cylinder Line, Root-Line,
SCREW-LINE, SCREW-LINE Promote plus, iSy,
CAMLOG Biotechnologies, Basel, Switzerland),
ITI and Straumann implants (Straumann, Basel,
Switzerland), FRIALIT 2 (Dentsply Sirona, Mannheim, Germany), XiVE (Dentsply Sirona), ASTRA
TECH OsseoSpeed (Dentsply Sirona), IMZ TwinPlus (Dentsply Sirona) and ANKYLOS (Dentsply
Sirona). If necessary, bone augmentation procedures were performed before or during the implantation. After completion of the healing
phase, the patients were referred back to their
dentists or prosthodontists for further prosthetic treatment and follow-up. Later on, some of
those patients were referred to our practice
again because of periimplantitis.
Therapy

Before periimplantitis treatment, clinical and
radiographic evaluation took place. In the case
of acute inflammation, anti-inflammatories
were locally applied. Patients underwent professional tooth cleaning and periodontal therapy
in the case of generalized periodontitis.
Periimplantitis was classiﬁed and treated in
accordance with Schwarz et al. (Fig. 1).17, 18 After
exposing the defects and removing granulation
tissue, implantoplasty was performed using diamonds rotary instruments and Arkansas stones
ﬁnishing burs. Defects were cleaned with sterile saline. Intraosseous defects (defect Classes Ib,
c, d and e; Fig. 1) were augmented according to
the treatment protocol using a DBBM (Geistlich
Bio-Oss spongiosa granules, Geistlich Pharma,
Wolhusen, Switzerland) and an NBCM (Geistlich
Bio-Gide Perio, Geistlich Pharma). The surgical
area was carefully closed, a periodontal wound
dressing applied (Coe-Pak, GC Europe, Leuven,
Belgium) and a radiographic evaluation performed. Patients were advised to rinse cautiously
with chlorhexamed 0.2% (GSK, London, U.K.)
from the ﬁrst day postsurgery for one week.
Antibiotics were given at the discretion of the
Materials and methods
surgeon starting 24 h before surgery until suture
removal eight days postsurgery. Patients were
Study population
followed up according to a strict recall schedule
The retrospective evaluation included 107 pa- in our practice. If necessary, supplementary
tients with 158 implants that were treated for therapy, such as gingivectomy or implantoplasperiimplantitis between 2009 and 2015. Im- ty, was performed during the follow-up phase.
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Guided bone regeneration in periimplantitis therapy

Fig. 1

Fig. 1
Defect classes and treatment
protocol according to Schwarz
et al.17, 18
Ia (buccal vertical bone
dehiscence),
Ib (buccal dehiscence and
semicircular bone defect to
the middle of the implant
body),
Ic (buccal dehiscence,
circular bone defect,
maintained lingual solid bone),
Id (buccal and lingual
dehiscence defects),
Ie (circular bone resorption,
buccal and oral compacta
maintained),
II (supra-alveolar
circumferential bone loss).

In an additional subanalysis, implants inserted
between 1993 and 2014 were evaluated for priBoth hopeless implants extracted before the mary indication classes and the rate of explanperiimplantitis therapy and implants treated by tations.
a different dentist with incomplete data were
not included in our evaluation. Data for the clinStatistical analysis
ical evaluation were retrieved retrospectively
from the patient ﬁles in our practice and includ- The following exploratory tests were performed:
ed plaque index, full-mouth bleeding on probing
(BOP) and probing pocket depth (PPD). PPD was – To test the null hypothesis of no association
measured from the mucosal margin to the botbetween indication class and the need for imtom of the probeable pocket mesially, distally,
plant therapy, the approximate chi-squared
orally and vestibularly at the start of the periimtest for association was used. The signiﬁcance
plantitis therapy and during recall visits in our
level was set at 5%.
practice at 3, 6, 9, 12, 24, 36, 48 and 49 to 56 – All pairs of indication classes were tested
months. In order to evaluate possible risk factors
against each other using the same chi-squared
for periimplantitis, signs of prosthetic deﬁcientests. In order to avoid inﬂation of Type I error
cies at the start of the therapy were analyzed,
due to multiple testing, all p-values were
as was history of periimplantitis. Additionally,
multiplied by the number of such comparisons
patient ﬁles were analyzed to identify smoking,
(15; Bonferroni correction).
bisphosphonate intake and diabetic patients at – Each indication class was compared to all oththe time of implantation.
er indication classes pooled using the chiIn order to analyze the prevalence of periimsquared tests already mentioned above. Since
plantitis per indication, implants were allocated
there were six comparisons, p-values were
to one of the following indication classes as demultiplied by six (Bonferroni correction) to
ﬁned at the consensus conference of the BDIZ
account for multiple testing.
EDI, DGI, DGMKG, DGZI and BDO (national
German dental associations) on Oct. 8, 2014:
– Ia: single-tooth replacement in the anterior
Results
area;
– Ib: single-tooth replacement in the posterior Between 1993 and 2014, a total of 22,724 imarea;
plants were inserted in 9,429 patients in our
– IIa: interdental space;
practice and patients were then referred back
– IIb: free-end situation;
to their prosthodontists or treating dentists for
prostheses. During the observation period of our
– IIc: greatly reduced residual dentition; and
– III: edentulous jaw.
evaluation (2009–2015), 516 of those patients
Analysis

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Guided bone regeneration in periimplantitis therapy

Fig. 2

Fig. 2
Time after implantation in
years at start of periimplantitis
therapy.
(NA = unknown; n = 158).

with a total of 637 implants were referred back
to our practice owing to periimplantitis. Of
these, 471 implants were deemed hopeless and
extracted immediately (73.9%). Eight implants
for which periimplantitis therapy was planned
had to be extracted at the start of the treatment
phase. Thus, periimplantitis therapy was initiated for 158 implants in 107 patients (24.8%).
Analysis of the original patient ﬁles established
that cemented reconstructions were used in 128
implants (77.6%) and screw-retained reconstructions in 37 implants (22.4%). The 158 implants had been in place for nine months to
15 years (Fig. 2). Most of the periimplantitis
infections had occurred within the first five
years after implant insertion (108 implants;
68.4%). In one implant, this period was retrospectively not clearly determinable. Seventytwo implants treated with periimplantitis
therapy were located in the maxilla (45.6%) and
86 in the mandible (54.4%). The distribution of
the implantation sites is shown in Figures 3a
and b. Before the observation period of our evaluation, 17 implants had been explanted owing
to periimplantitis and replaced (10.8%). The
newly inserted implants developed periimplantitis again.
Of the patients referred back to our practice
and treated for periimplantitis, 41 were male
(38.3%) and 66 were female (61.7%). The mean
age of the 107 patients at the start of the periimplantitis therapy was 58 ± 11 (23–85) years. At
the time of implantation, 18 of the 107 patients

were smokers (16.8%), three had received bisphosphonate treatment (3.80%), ﬁve had diabetes mellitus (4.67%) and 81 did present any
conspicuous medical ﬁndings (75.7%), based on
the original patient ﬁles. The following prosthetic deﬁciencies of the implants were identiﬁed in
25 of the 107 patients (36%): formation of marginal gaps, overcontouring, overload, insufficient
biological width, unnecessary splinting and
cement residue.
In 52 of the 107 patients (48.6%), generalized
periodontitis was diagnosed for 79 implants
(50.0%) and treated accordingly. The distribution of the periimplantitis defect classes is
shown in Figure 4. In 45 implants (28.5%), the
therapy included GBR using a DBBM and an
NBCM. The remaining 113 implants underwent
professional tooth cleaning and were treated
according to the implantoplasty protocol. At the
start of the periimplantitis therapy, the BOP of
the 158 implants was 100.0% and the plaque
index was on average 48.5 ± 26.6% (n = 88).
After initiation of the periimplantitis therapy,
the mean vestibular PPD of the 158 implants
was reduced from 4.93 ± 1.94 mm to
2.67 ± 0.88 mm after 12 months (n = 123) and
2.71 ± 0.30 mm after 49–56 months (n = 32;
Figs. 5a & b), therefore on average below the
level stated for the deﬁnition of periimplantitis.9
Stable PPD reduction was also found for implants with long-term follow-up data 49–56
months post-therapy (Fig. 6). BOP was absent
in 50.0% of 58 analyzed implants at 12 months

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Guided bone regeneration in periimplantitis therapy

Fig. 3a

Figs. 3a & b
Number of affected implants
per site: (a) maxilla
(b) mandible. (n = 158).
Fig. 4
Defect classes at the start
of periimplantitis therapy
according to Schwarz et al.17, 27
Figs. 5a & b
(a) Box plot of pocket depth
preoperatively and three,
six, nine and 12 months after
the start of periimplantitis
therapy. (m = mesial;
v = vestibular; d = distal;
o = oral; n = 123–158).
(b) Box plot of pocket depth
after 24, 36, 48, and 49
and more months after the
start of periimplantitis
therapy. (m = mesial;
v = vestibular; d = distal;
o = oral; n = 16–158).

Fig. 3b

Fig. 4

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Guided bone regeneration in periimplantitis therapy

Fig. 5a

Fig. 5b

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Guided bone regeneration in periimplantitis therapy

Fig. 6

Fig. 6
Pocket depth after 49 and
more months compared with
pocket depth at 12 months
in all treated implants.
(m = mesial; v = vestibular;
d = distal; o = oral;
12 months: n = 158; 49 and
more months: n = 16).
Fig. 7
Number of implants showing
BOP before periimplantitis
therapy and at recall visits up
to 49 and more months after
the start of the therapy.
(n = 8–158).

Fig. 7

after the periimplantitis therapy and in 73.1% of
26 implants evaluated with long-term data
available 49–56 months post-therapy (Fig. 7).
During the follow-up period, one treated implant had to undergo additional gingivectomy
and eight repeated implantoplasties. Despite
treatment, 15 implants had to be explanted
38 Volume 3 | Issue 1/2017

during the follow-up period (9.49%), three of
these in patients with diabetes, one in a smoker
and two in which the therapy included an
intraosseous defect treatment.
Evaluation of the original data ﬁles for the
158 treated implants established that bone augmentation procedures using a DBBM and an

Journal of
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Guided bone regeneration in periimplantitis therapy

Table 1

Number of implants
inserted

Number of
explantations

% loss due to
explantations

ANKYLOS

191

5

2.62

ASTRA TECH

1177

21

1.78

CAMLOG .Cylinder Line

4888

578

11.80

CAMLOG Screw Cylinder Line

1783

63

3.53

CAMLOG ROOT-LINE

289

21

7.27

CAMLOG SCREW-LINE

747

34

4.55

CAMLOG SCREW-LINE Promote plus

8014

105

1.31

CAMLOG iSy

62

2

3.23

Dentegris

6

FRIALIT 2

2042

234

11.50

IMZ TwinPlus

499

67

13.40

ITI

37

1

2.70

Nobel

11

Straumann

324

30

9.26

XiVE

2430

53

2.18

Others

155

15

9.68

Implant type not classiﬁed

69

10

14.50

22724

1239

5.45

Implant system

Total

NBCM had been performed in 20 implants
(12.7%) before or simultaneously with the implantation. Autologous bone had been used additionally for one of these. No initial augmentation had been performed in 127 implants (80.4%),
while this information was not available for 11
implants (6.96%). The augmentation rate of all
22,724 implants inserted between 1993 and
2014 was 31%. In an additional subanalysis, for
all 22,724 implants, the explantation rate was
evaluated per implant system (Table 1). Of these,
1,239 implants were explanted owing to periimplantitis (5.45%). The highest rates of explantations were noted for the CAMLOG Cylinder Line,
FRIALIT 2 and IMZ TwinPlus.
Statistical analysis of the null hypothesis of
no association between indication class and the
need for implant therapy applying the chisquared test yielded a p-value of 0.0056. Thus,
at the 5% level of signiﬁcance, the hypothesis
of no differences across indication classes with
respect to the need for periimplantitis therapy
might be withdrawn. Comparing the implant
indication classes between all 22,724 implants
and the 158 implants that underwent periimplantitis therapy, free-end situations (indication
Class IIb) tended to be more frequent in the
periimplantitis group (p = 0.07), while interden-

0.00

0.00

tal spaces (indication Class IIa) were signiﬁcantly
less frequent (p = 0.02). The frequencies of all
other indication classes were not signiﬁcantly
different between all inserted implants and implants that underwent periimplantitis therapy
(Fig. 8). However, in 2,728 of all 22,724 inserted
implants (12%), the indication class could not be
evaluated retrospectively.

Discussion
The retrospective evaluation presented here
focused on the treatment of patients with implants placed between 1993 and 2014 in our
practice and later treated again owing to periimplantitis. Of the implants that received periimplantitis therapy with or without GBR, treatment
was successful in terms of stable reduction in
PPD and BOP and implant survival of 90.5%, as
only 15 of the 158 implants had to be extracted
despite periimplantitis therapy over the observation period of our evaluation.
Our ﬁndings are in accordance with several
reviews reporting successful surgical therapy
of periimplantitis despite disease progression or
recurrence.7, 10, 19, 20 A recent meta-analysis compared the results for PPD reduction and radio-

Journal of
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Table 1
Distribution of implant
systems: overall inserted
implants and implants
affected by periimplantitis
between 1993 to 2014.

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Guided bone regeneration in periimplantitis therapy

Fig. 8

Fig. 8
Distribution per indication
class at the time of implantation for implants treated for
periimplantitis compared with
all inserted implants.
(All implants: n = 22,724;
periimplantitis-affected
implants: n = 158).

graphic bone ﬁll for different surgical approaches.19 Greater PPD reduction and radiographic
bone ﬁll were found when grafting materials
and membranes were applied compared with
procedures that used access ﬂaps, debridement
and resection. In another meta-analysis, greater PPD reduction and gain of clinical attachment
were found when bone grafts and membranes
were applied compared with a nonsurgical therapy.21 However, regenerative therapy has been
shown to be more effective in contained, circumferential intrabony defects than in defects
with buccal dehiscences or a predominantly
suprabony component.11 Therefore, in our evaluation, a treatment concept considering defect
morphology according to the classiﬁcation of
Schwarz et al. was applied.17, 18 Interestingly,
36.1% of the implants with periimplantitis presented with a defect morphology allowing bone
augmentation procedures. For ﬁnancial reasons,
in only 28.5% of the implants did periimplantitis
therapy include bone augmentation. This included defect Classes Ib, c, d and e. The defect morphology of the remaining implants treated for
periimplantitis corresponded to 55.0% Class II
and 8.9% Class Ia defects. These defect types
were therefore treated by anti-infective, resective therapy only.
For the regenerative treatment of intraosseous defects, we applied a DBBM and an NBCM.
Our ﬁndings are in accordance with other reports
that found encouraging results of periimplantitis treatment using a DBBM with or without an
40 Volume 3 | Issue 1/2017

NBCM. In a case series of 51 consecutively treated patients who presented with periimplantitis,
Froum et al. used enamel matrix protein, a combination of a platelet-derived growth factor with
anorganic bovine bone or mineralized freezedried bone and an NBCM.14 Bone level measured
by periapical radiographs or bone sounding increased and remained stable up to 7.5 years
after periimplantitis therapy. Positive results in
terms of PPD reduction and radiographic bone
ﬁll after one year were also found using a DBBM
and an NBCM in intrabony defects with a
PPD > 5 mm.15 Using a DBBM, Aghazadeh et al.
reported reduced PPD after 12 months and a
higher likelihood of radiographic defect ﬁll compared with autogenous bone.13 In two other
studies, a significant defect reduction was
achieved using a DBBM in implants with craterlike defects at the one-year follow-up.12, 16 These
results, together with the data of our retrospective evaluation, demonstrate that periimplantitis treatment using a DBBM and an NBCM in
defects with suitable defect morphologies may
be clinically effective.
In our retrospective evaluation, only a quarter of the implants affected by periimplantitis
underwent therapy while all other implants were
regarded as hopeless and explanted. We support
recommendations of other authors to include
patients with implants in a strict maintenance
program7, 8 as poor oral hygiene is a well-known
risk factor for periimplantitis.6 However, this was
probably not ensured in many of the cases

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Guided bone regeneration in periimplantitis therapy

included in our evaluation, as almost half of the
patients presented with generalized periodontitis at the start of the periimplantitis treatment.
Therefore, periimplantitis may have proceeded
in many implants to a stage that required explantation. In fact, a recent analysis demonstrated that implants provided with prostheses
delivered by general practitioners were at higher
risk of moderate and severe periimplantitis.22
Dentists who follow up on implant patients
should be sensitized and should be instructed
to establish strict maintenance programs according to consensus statements, especially
regarding diagnosis of mucositis. Regular clinical monitoring with professional plaque removal and reinforcement of oral hygiene may also
have been a main factor of the long-term success of the 158 implants that received periimplantitis therapy in our evaluation.
Simultaneous bone augmentation procedures at the time of implantation may bear higher risk of periimplantitis.23, 24 The results of our
retrospective evaluation, however, established
that only 12.7% of the implants that received
periimplantitis therapy had initially been inserted together with bone augmentation. Bone
augmentation in all 22,724 inserted implants
was 31%. The results indicate that implants in
augmented sites are not more susceptible to
periimplant infection than implants inserted
without bone augmentation. Nevertheless,
clear conclusions must ﬁrst be drawn in clinical
studies including both hopeless implants and
implants suitable for periimplantitis therapy.
Various clinical studies have found smokers
to be at higher risk of developing periimplant
infections.6, 25 A meta-analysis by Atieh et al.
found a signiﬁcantly higher frequency of periimplant disease in smokers (36%).2 This is in accordance with the results of our retrospective
evaluation, in which 16.8% of the patients who
underwent periimplantitis therapy were smokers and 16.7% of the smokers had already
undergone explantation and re-implantation
previously. Uncontrolled diabetes and the intake
of bisphosphonates are two additional risk factors for periimplantitis.6, 25 In our retrospective
evaluation, 4.67% of the patients were diabetic and 3.80% received bisphosphonates at the
time of implantation. Lindhe et al. demonstrated that 5% of the patients that had undergone
periimplantitis therapy and 23% of the patients
in which explantations were performed despite
the therapy had diabetes.6 These results support the conclusion that implant patients with

diabetes are at higher risk and should be informed accordingly. Similarly, bisphosphonates
have been found to increase the risk of implant
failure due to impaired implant osseointegration. However, a review has shown that successful long-term results of implant therapy can be
achieved in patients despite bisphosphonate
intake.26 Our retrospective evaluation, however,
does not provide a clear conclusion for negative
effects of bisphosphonate intake or diabetes
mellitus on the long-term survival of implants.
In an additional subanalysis, the overall explantation rate of implants placed between
1993 and 2014 was calculated to be 5.45%.
Three implant systems presented with a failure
rate of more than 10%. However, the number
of periimplantitis patients who were not referred back and treated elsewhere is not known.
Therefore, the analysis does not allow for deﬁnitive conclusions of the prevalence of periimplantitis affecting implants inserted in our practice.

Conclusion
In our retrospective evaluation, data from patients who were referred for periimplantitis
treatment were analyzed. Using a treatment
approach that included a hygiene phase and that
considered defect morphology, PPD and BOP
were improved and remained stable over more
than four years post-therapy. Retreatments or
explantations may be necessary and should be
considered part of periimplantitis therapy. The
results of our evaluation demonstrated that
periimplantitis can be treated successfully and
with good long-term results if a treatment approach is chosen based on defect morphology
and on consensus recommendations and if patients are enrolled in a strict maintenance program. However, owing to the retrospective
character of this evaluation, it is recommended
that scientiﬁcally sound clinical trials be performed to further evaluate the efficacy of the
periimplantitis treatment described here.

Competing interests
The expenses for statistical data analysis and
description were covered by Geistlich Pharma,
Wolhusen, Switzerland. Other than that, the
authors declare that they have no competing
interests.

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Froum SJ, Froum SH, Rosen PS. Successful
management of peri-implantitis with a
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8.
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15.
Matarasso S, Iorio Siciliano V, Aglietta M,
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Roccuzzo M, Gaudioso L, Lungo M,
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Canullo L, Tallarico M, Radovanovic S,
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2010 Apr;81(4):479–84.
27.
Schwarz F, Sahm N, Becker J. Impact of
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World Oral
Health Day
20 March

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B o n e a u g m e n t a t i o n u s i n g p o r o u s ʸ -TC P B o n e a u g m e n t a t i o n o f c a n i n e f r o n t a l s i n u s e s u s i n g a p o r o u s ʸ-t r i c a l c i u m p h o s p h a t e

Bone augmentation of canine
frontal sinuses using a
porous ʸ-tricalcium phosphate
for implant treatment
Abstract
Objective
Masataka Hirose,a Naoya Uemura,a Yoshiya Hashimoto,b
Isumi Todac & Shunsuke Babaa
a

Department of Oral Implantology, Osaka Dental
University, Hirakata, Japan
b
Department of Biomaterials, Osaka Dental University,
Hirakata, Japan
c
Department of Anatomy, Osaka Dental University,
Hirakata, Japan

Corresponding author:
Dr. Yoshiya Hashimoto
Department of Biomaterials
Osaka Dental University, 8-1
Kuzuhahanazono-cho Hirakata
5731121 Osaka
Japan
yoshiya@cc.osaka-dent.ac.jp

Compared with hydroxyapatite, alpha-tricalcium phosphate (͂-TCP) is
more biodegradable and shows better integration during physiological
bone remodeling. The objective of this study was to evaluate the effects
of porous ͂-TCP as a tissue-engineered scaffold for maxillary sinus augmentation in a canine model.
Materials and methods

Porous ͂-TCP was prepared by pulverizing an ͂-TCP block with an 80%
continuous pore structure. Bilateral sinus ﬂoor augmentation surgeries
were performed on beagle dogs that were randomly divided into two
groups based on the type of repair: The experimental group received a
porous ͂-TCP and titanium (Ti) implant, and the control group received
a Ti implant. Periimplant bone volume (BV) and bone mineral content
(BMC) were measured and analyzed using micro-computed tomography
(micro-CT) and Villanueva–Goldner staining for histological examination.
The intergroup differences were evaluated using the Student’s t-test.

How to cite this article:
How to cite this article: Hirose M, Uemura N, Hashimoto Y,
Toda I, Baba S. Bone augmentation of canine frontal
sinuses using a porous ʸ-tricalcium phosphate for implant
treatment.
J Oral Science Rehabilitation.
2017 Mar;3(1):44–51.

Results

Micro-CT images at 12 weeks after surgery showed higher BV and BMC
in the experimental group than in the control group (p < 0.05). Histological examination showed high levels of ͂-TCP even at four weeks, but
the scaffolds were completely absorbed and new bone integrated into
the Ti implants at 12 and 24 weeks. However, no bone formation was
observed in the control group throughout the study.
Conclusion

Porous ͂-TCP increased BV and promoted bone mineralization and earlier bone formation in the augmented maxillary sinus. Therefore, this
tissue-engineered scaffold might be a better alternative to autologous
bone for maxillary sinus augmentation.
Keywords

Bone augmentation, porous ͂-tricalcium phosphate, canine frontal
sinuses.

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Introduction

Materials and methods

Implant placement in highly atrophic maxillae has
been a major challenge in implant dentistry. Sinus
ﬂoor elevation is a preferred option in such situations. Various maxillary sinus ﬂoor augmentation techniques have been developed for managing severe bone loss in the maxilla.1–4 However, it
is important to deﬁne the best bone substitute
for the subsinus cavity after sinus membrane lift
procedures. Although autogenous bone grafting
is still considered the gold standard for treatment,
it has several disadvantages, including the requirement of a second surgery at the donor site
and limited bone supply.5, 6 Artiﬁcial bone grafts
are promising alternatives to autogenous bone
grafts.
Synthetic hydroxyapatite (HA) has been
widely applied in the medical and dental ﬁelds
because of its high biocompatibility and osteoconductive properties.7, 8 However, the application
of HA has to be carefully considered because it is
poorly displaced by new bone tissue9 and is easily
adsorbed by bacteria and epithelial cells because
of its high surface energy.10, 11 Bovine HA is frequently used as a grafting material in sinus lift
procedures because of its features that resemble
cancellous bone, complete deproteinization of the
inorganic component and thus the absence of
antigenicity.12 Beta-tricalcium phosphate (ʹ-TCP)
was one of the earliest calcium phosphate compounds used as a bone graft substitute because
of its high osteoconductivity, tissue compatibility
and ability to withstand sufficient mechanical
stress.13 High-temperature TCP, known as ʸ-TCP,
is often prepared by sintering amorphous precursors with the proper composition.14
Marukawa et al. demonstrated the usefulness
of self-setting ʸ-TCP (BIOPEX-R) in maintaining
the rigidity of implanted bone screws using maxillary sinus augmentation in rabbits.15 However, a
drawback of self-setting bone cement is its weak
mechanical property. In a previous study, we fabricated porous ʸ-TCP composites with a continuous small-and-large-pore structure and demonstrated that the composite created using porous
ʸ-TCP particles and collagen or collagen model
peptide had enough adaptability for treating skull
bone defects in miniature pigs.5 However, the
effectiveness of porous ʸ-TCP particles as a grafting material in sinus lift procedures has not yet
been investigated. The objective of this study was
to evaluate the effects of porous ʸ-TCP as a
tissue-engineered scaffold using a canine frontal
sinus model.

Material analysis

Preparation and characterization of porous
ʸ-TCP particles
Porous ʸ-TCP particles with an average diameter of 580.8 μm and porosity of about 80% were
obtained from Taihei Chemical Industrial (Osaka,
Japan) and sterilized by dry heating before the
experiment. A ﬁeld-emission scanning electron
microscope (S-4100, Hitachi High-Technologies
Corporation, Tokyo, Japan) was used to analyze
particle size, pore distribution and outer surface
conditions. Before observation, samples were
coated with platinum–palladium using the
E-1030 (Hitachi High-Technologies Corporation).
ʸ -TCP particles were characterized using a
powder X-ray diffraction system (XRD; XRD6100, Shimadzu, Kyoto, Japan). XRD patterns
were obtained with the following parameters:
40 kV, 30 mA, scan rate of 2°/min and step size
of 0.05° within a range of 10–60°. Crystal phase
was characterized using data from the International Centre for Diffraction Data (HA: 9-0432;
ʸ-TCP: 9-0348). X-ray photoelectron spectroscopy (XPS) measurements were performed to
determine the surface Ca/P atomic ratios with
a PHI X-tool (Ulvac-Phi, Chigasaki, Japan)
equipped with an Al–Kʸ radiation source (15 kV;
53 W; spot size of 205 μm) at a pass energy of
280.0 eV, a step size of 0.1 eV and a takeoff angle
of 45° with 20 scans.
Animal models

The mandibular defect model was established
using six healthy beagles (2 years old; weighing
approximately 10 kg) obtained from Hamaguchi
Animal (Osaka, Japan). The animals were housed
in a temperature-controlled environment at
24 °C with free access to food and water. The
body weight and general health of the animals
were monitored throughout the study.
ʸ- T C P p a r t i c l e t r a n s p l a n t a t i o n

The dogs underwent bilateral sinus floor
augmen tation surgeries and were randomly
divided into two groups depending on the type
of repair: The experimental group received a
porous ʸ-TCP and tapered titanium (Ti) implant
(NovelActive, Nobel Biocare Japan, Tokyo,
Japan), and the control group received the

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Figs. 1a & b

Figs. 1a & b
Scanning electron micrograph
of porous ʸ-TCP particles:
(a) low-magniﬁcation image;
(b) high-magniﬁcation image.

Ti implant alone. All procedures in this study
were approved by the Animal Experiment Committee of Osaka Dental University and conformed to the Guiding Principles for the Use of
Laboratory Animals (approval No. 14-03015).
Aseptic surgery was performed under general
anesthesia (0.5 mg/kg pentobarbital sodium)
with physiological saline cooling and inﬁltration
anesthesia (1.8 mL of 2% lidocaine hydrochloride
and 1:80,000 epinephrine). The hair from the
frontal region was removed, and the skin including the frontal sinus was incised in the shape of
an arc. The skin–periosteal ﬂap was detached,
and the anterior wall of the frontal sinus was
exposed. Then, an approximately 10 mm wide
rectangular opening was made in the anterior
wall of the left and right frontal sinuses using a
twist drill (Astra Tech, Tokyo, Japan). In addition,
porous ʸ-TCP particles (2.7 cm3) were ﬁlled in
this elevation space. The Ti implant was embedded at a distance of about 5 mm from the bony
window. The anti-inﬂammatory agent carprofen
(Carprodyl VR, Ceva, Libourne, France) was administered daily for seven days after the surgery.
Radiographic analysis

The maxillae were harvested for examination by
micro-computed tomography (micro-CT; SMX130CT, Shimadzu). Blocks of bone specimens
were mounted on the turntable and scanned at
105 kV and 30 μA. TRI/3D-BON software
(RATOC System Engineering, Tokyo, Japan) was
used to generate a 3-D reconstruction using the
volume-rendering method for morphological
assessment. In the 3-D analysis, bone volume
(BV in mm3) and bone mineral content (BMC in
46 Volume 3 | Issue 1/2017

mg) were measured using the TRI/3D-BON software based on the values obtained.
Histological assessment

After fixation with 10% phosphate-buffered
formalin, the specimens with the Ti implant were
dehydrated in ethanol and then embedded in
acrylic resin (Technovit 7200 VLC, Heraeus
Kulzer, Wehrheim, Germany). The embedded
blocks were trimmed using a cutter and ground
using abrasive paper. Thereafter, the sections
were further ground to a ﬁnal thickness of about
30 μm. Finally, the specimens were stained with
the Villanueva–Goldner stain and examined
under a microscope.

Results
Characterization
o f ʸ- T C P p a r t i c l e s

Figure 1 shows the electron micrographs of
ʸ-TCP particles. At low magniﬁcation, the ʸ-TCP
particles had an amorphous body with many
small and large pores (Fig. 1a). At high magniﬁcation, the ʸ-TCP particles had smooth surfaces with a pore diameter of approximately
5–10 μm. The XRD proﬁles of both intact particles are shown in Figure 1b. The speciﬁc peaks
of ʸ-TCP (indicated by the triangles) were detectable in the XRD patterns of both particles
(Fig. 2). For XPS, quantitative data of the atom%
were obtained from the peak areas derived for
O1s, Ca2p, P2p and C1s, from which the Ca/P
ratio was calculated and found to be 1.5 (Fig. 3).

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Fig. 2

Fig. 2
XRD pattern of porous
ʸ-TCP particles. Triangles
show ʸ-TCP peaks.
Fig. 3
Wide X-ray photoelectron
spectra of porous
ʸ-TCP particles.

Fig. 3

Radiographic analysis

BV and BMC analysis

A quantitative imagology analysis of the bone
window areas of the specimens was carried out
at four, 12 and 24 weeks using micro-CT (Fig. 4).
In the experimental group, newly formed bone
was observed in the area of the bone window;
however, bone formation reduced between 12
and 24 weeks. In the control group, the area of
the bone window was empty, although some
new bone formation was observed toward the
edges of the bone window.

BV and BMC of each group were determined at
four, 12 and 24 weeks (Fig. 5). BV and BMC were
higher in the experimental group than in the
control group at 12 weeks (p < 0.05). No significant intergroup differences were observed in
either analysis at four or 24 weeks (p > 0.05;
Fig. 5).

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Fig. 4

Fig. 5

Fig. 4
Micro-CT images acquired
at four, 12 and 24 weeks after
surgery. (PA = palatal side;
NA = nasal side).
Fig. 5
The upper and lower groups
show BV (mm3) and BMC (mg)
of each group, reﬂecting the
quantity of new bone at four,
12 and 24 weeks after surgery.

Histological assessment

Histological assessments were also performed
at four, 12 and 24 weeks (Figs. 6 & 7). Histological images showed high levels of porous ʸ-TCP
even at four weeks; however, the scaffolds had
completely absorbed and new bone integrated
into the Ti implants at 12 and 24 weeks. The
48 Volume 3 | Issue 1/2017

formation of new bone in the area of the bone
window reduced between 12 and 24 weeks;
however, the newly formed bone had changed
to mature bone (Fig. 6). Although no bone formation was observed in the control group
throughout the study, some new bone formation
was observed toward the edges of the bone window (Fig. 7).

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B o n e a u g m e n t a t i o n u s i n g p o r o u s ʸ -TC P B o n e a u g m e n t a t i o n o f c a n i n e f r o n t a l s i n u s e s u s i n g a p o r o u s ʸ-t r i c a l c i u m p h o s p h a t e

Fig. 6

Fig. 6
Low- and high-magniﬁcation
images in the experimental
group, demonstrating new
bone formation in the upper
and lower groups at 4, 12 and
24 weeks after surgery.
Red asterisks show the
residual porous ʸ-TCP
particles. Each black bar of
the low- and highmagniﬁcation images shows
1,000 and 500 μm,
respectively.
Fig. 7
The low- and highmagniﬁcation images in the
control group, demonstrating
new bone formation in the
upper and lower groups at
4, 12 and 24 weeks after
surgery. Each black bar of the
low- and high-magniﬁcation
images shows 1,000 and 500
μm, respectively.

Fig. 7

Discussion
ʸ-TCP is widely considered an option for use as
a bone grafting material. However, few studies
have used porous ʸ-TCP particles for sinus lift
with tissue engineering techniques. In order
maximize the surface area for cell attachment
and proliferation, we fabricated the scaffold into

a highly porous 3-D structure through a relatively simple processing method involving a
conventional sintering procedure. Previous studies have used a slurry of ʹ-TCP and potato starch
to produce ʸ-TCP that was in a thermodynamically stable phase at temperatures above
1,100 °C.16 Uchino et al. found that HA formation
is rarely observed on the surface of porous ʸ-TCP

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ceramics with 80% porosity.17 In this study, a
comparison of the scatter plot data of the synthesized ʸ-TCP particles with that of ʸ-TCP data
registered with the Joint Committee on Powder
Diffraction Standards confirmed that these
peaks appeared at the same angles. In addition,
the Ca/P ratio of the product was 1.5, which fulﬁlled the requirements of the ASTM standards.18
Basic animal research on sinus lift has been
conducted on dogs, sheep and rabbits.12, 19, 20 The
canine frontal sinus is a size closer to the human
maxillary sinus and allows accurate control of a
large number of experimental models. In addition, the canine frontal sinus is the largest
among the canine paranasal sinuses and the
canine sinus wall is covered with multiple rows
of ciliated columnar epithelium, as is the human
maxillary sinus. 21 Moreover, the surgeon can
approach both sides of the frontal sinus through
a single incision because the left and right frontal sinuses are adjacent to each other.
In the edentulous jaw and sinus-alveolar
crest, the distance between the sinus and the
alveolar bone is important in terms of implant
treatment. A bone height of around 20 mm is
required for dental implant treatment; therefore,
sinus surgery is expected to promote bone formation to a height of more than 20 mm.22 Since
the vertical length of the human maxillary sinus
is about 28 mm, the top of the implant projects
from the maxillary sinus ﬂoor into the elevation
space of 20 mm.21 In this experiment, the top of
the implant projected into the canine frontal
sinuses. Therefore, the canine frontal sinus was
considered a suitable experimental model of
sinus surgery.
The biological behavior of ʸ-TCP-based biomaterials has been analyzed in several in vivo
studies.23–25 Kihara et al. performed an in vivo
test using a rat model to observe the biodegradation process of particles (~300 μm diameter)
of pure ʸ-TCP and found that the residual ʸ-TCP
particles degraded without decreasing the
volume of the transplantation region.26 Our previous study evaluated the effects of combining
poly(Pro-Hyp-Gly) and ʸ-TCP particles on bone
formation in a canine tibial defect model.23 These
particles did not induce inﬂammation; moreover,
complete degradation and remodeling of the
lamellar bone were observed with their use.
This, to our knowledge, is the first study to
inves tigate the effects of porous ʸ-TCP as a
tissue-engineered scaffold for maxillary sinus
augmentation in a canine model. Although histological images showed high levels of porous
50 Volume 3 | Issue 1/2017

ʸ-TCP at four weeks, new bone formation had
already started. Moreover, the porous ʸ-TCP
particles had been completely absorbed and
replaced with new bone at 12 weeks. New bone
formation in the area of the bone window reduced between 12 and 24 weeks. No bone exists
originally in the area of the bone window; thus,
the newly formed bone will be absorbed over
time. Mechanical stresses, such as occlusion,
may inhibit the absorption of the newly formed
bone. Although ʹ-TCP was an acceptable bone
substitute material for augmenting maxillary
sinus bone formation, it was likely to continue
increasing and would have been progressively
replaced over a longer time. 27 However, prolonged bone augmentation is disadvantageous.

Conclusion
Sinus ﬂoor augmentation is a safe and elegant
surgical procedure before implant insertion. The
porous ʸ-TCP tested is a biocompatible, osteoconductive material that promotes new bone
formation when used with integrated Ti implants, as demonstrated in this study on a canine
frontal sinus model. However, the effectiveness
and safety of this method need to be further
evaluated before it can be clinically applicable.

Competing interests
The authors declare no conﬂicts of interest.

Acknowledgments
This work was funded by the Promotion and
Mutual Aid Corporation for Private Schools of
Japan’s Science Research Promotion Fund
(Tokyo, Japan; No. 15-09).

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Matsuno T, Nakamura T, Kuremoto K,
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Shimizu H, Watanabe T, Sato J.
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Evaluation of surgical difficulty of extraction

Importance of a preoperative
radiographic scale for evaluating surgical
difficulty of impacted mandibular third
molar extraction
Abstract
Objective
Natalia Ribes Lainez,a José Carlos Sanchis Gonzáleza,
David Peñarrocha Oltraa & José María Sanchis Bielsaa, b
a

Department of Stomatology, Faculty of Medicine and
Odontology University of Valencia, Valencia, Spain
b
Department of Stomatology and Maxillofacial Surgery,
General University Hospital of Valencia, Spain

Corresponding author:
Dr. David Peñarrocha Oltra
Cirugía Bucal. Clínicas Odontológicas
C/Gascó Oliag, 1
46021 Valencia
Spain
T +34 963 86 4144
david.penarrocha@uv.es

The objectives of the study were to evaluate the correlation between the
degree of surgical difficulty measured by an established scale and the
total surgical time, the ostectomy time and the tooth sectioning time,
and to analyze which of the factors involved had a greater inﬂuence on
total surgical time.
Materials and methods

A presurgical radiographic scale was developed, based on ten parameters.
Each parameter was scored from 1 to 3, and the individual scores were
summed. A retrospective analysis using panoramic radiographs was
performed of patients subjected to surgical extraction of a mandibular
third molar, with recording of the surgical times. A statistical analysis
was performed to establish correlations between the study parameters
and scale and the surgical times.
Results

How to cite this article:
How to cite this article: Ribes Lainez N, Sanchis González
JC, Peñarrocha Oltra D, Sanchis Bielsa JM. Importance
of a preoperative radiographic scale for evaluating surgical
difficulty of impacted mandibular third molar extraction.
J Oral Science Rehabilitation.
2017 Mar;3(1):52–9.

A greater Winter’s distance prolonged ostectomy time and, conversely,
a greater distance from the mandibular ramus to the distal surface of the
second molar was observed to shorten ostectomy time. Separate or dysmorphic root shape increased ostectomy time and total surgical time.
Total surgical time was longer in the presence of greater coronal width
and a shorter distance from the ramus to the second molar. The only
variable correlated to tooth sectioning time was coronal width.
Conclusion

The ﬁnal score was correlated to ostectomy time and total surgical time.
Ostectomy time in turn was inﬂuenced by Winter’s distance, the distance
from the mandibular ramus to the second molar, and root shape. Tooth
sectioning time was inﬂuenced by the coronal width of the third molar.
The parameters with the closest correlation to total surgical time were
coronal width and the distance between the ramus and second molar.
Keywords

Third molar surgery, wisdom teeth, impacted mandibular third molar,
third molar extraction.
52 Volume 3 | Issue 1/2017

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Evaluation of surgical difficulty of extraction

Introduction
A number of classiﬁcation systems have been
proposed for estimating the surgical difficulty
of impacted mandibular third molar extraction,
based on preoperative assessment of panoramic radiographs. The traditional classiﬁcations are
those of Pell and Gregory1 and Winter,2 based
on the depth of the third molar, the relation to
the mandibular ramus and the anatomical position in relation to the longitudinal axis of the
adjacent second molar. Over the years, different
modiﬁcations of these scales have been proposed with the aim of improving the prediction
of surgical difficulty. In this regard, Pederson
proposed a modiﬁcation of the scale of Pell and
Gregory that contemplated an additional factor:
the position of the molar.3 Each variable was
assigned a score of 1–4 according to its inﬂuence
upon the difficulty of extraction, and these
scores were then summed to yield a ﬁnal score
predicting surgical difficulty: 3–4 (not difficult),
5–7 (moderate difficulty) and 7–10 (great difficulty). This scale has been widely cited in the
oral and maxillofacial surgical literature as an
easy way to predict the surgical difficulty of impacted mandibular third molar extraction.
Cáceres Madroño et al. added further parameters to the scale of Pedersen, such as mandibular height, distal inclination of the second
molar, size and shape of the dental follicle, and
development of the roots.4 Peñarrocha et al. in
turn summed the scores corresponding to pericoronal radiolucency, pericoronal space, Winter’s distance and coronal area, and subdivided
the size and shape of the roots into two separate
parameters: the length of the root and the type
of root.5 Each variable was scored from 0 to 2,
and the individual scores were summed to yield
a ﬁnal surgical difficulty score: 0–5 (not difficult), 6–10 (average difficulty) and over 10 (great
difficulty). This is one of the scales involving the
largest number of parameters, and higher scores
have been shown to correspond to longer ostectomy times and total surgical times—thereby
conﬁrming the efficacy of the classiﬁcation.5
Another clinical and radiographic scale for
predicting the difficulty of third molar extraction
was developed by Romero-Ruiz et al., based on
the classical parameters with the addition of
integrity of the bone and mucosa covering the
third molar.6 Minimum surgical difficulty was
predicted if the tooth was covered only by
mucosa, while maximum difficulty corresponded to molars fully covered by bone and mucosa.

Predicting the surgical difficulty of impacted
mandibular third molar extraction is essential
for treatment planning and helps assess professional surgical skill, reduces complications, optimizes patient preparation, and minimizes postoperative pain and inﬂammation.
The present study describes a radiographic
surgical difficulty scale based on a series of parameters and compares it with ostectomy time,
tooth sectioning time, the presence or absence
of additional ostectomy, and total surgical time.
In addition, actual measurements of the radiographic parameters were taken to identify those
that had the greatest impact upon surgical difﬁculty.

Materials and methods
A retrospective study using panoramic radiographs was conducted of patients subjected to
surgical extraction of an impacted mandibular
third molar in the Department of Stomatology
and Maxillofacial Surgery (General University
Hospital of Valencia, Valencia, Spain), with recording of the following surgical times: ostectomy time and tooth sectioning time (in seconds)
and total surgical time (in minutes), calculated
from the start of the incision to the last suture.
A presurgical radiographic scale was developed
(Figs. 1-10), based on ten parameters that were
recorded by three dental students of the Faculty of Medicine and Odontology, University of
Valencia, Valencia, Spain, using ImageJ software
(64-bit; developed by the U.S. National Institutes of Health, Bethesda, Md.)7, with calculation of the corresponding mean values: inclination of the third molar, inclination of the second
molar, pericoronal radiolucency, root radiolucency, root shape, Winter’s distance, distance between the ramus and second molar, width of the
third molar, coronal area and root length.
Calibration was carried out based on the calculation of the distortion of the radiographic
measurements versus the real measurements
of the third molar, using radiographic measurements of the diameter and length of 15 impacted mandibular third molars, exported to ImageJ,
and caliper measurements obtained after extraction of the third molar, respectively. The
statistical analysis of these dual measurements
(ImageJ and calipers) showed the distortion coefficient to be 0.11.
The ﬁnal score was obtained by summing
the individual scores for each parameter, coded

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Evaluation of surgical difficulty of extraction

Figs. 1a–c

a

b

c
Figs. 2a–c

a

b

c
Figs. 3a–c

a
Figs. 1a–c
Inclination of third molar:
(a) vertical (1);
(b) mesial (2); and
(c) distal or horizontal (3).
Figs. 2a–c
Inclination of second molar:
(a) mesial (1);
(b) vertical (2); and
(c) distal (3).
Figs. 3a–c
Pericoronal radiolucency:
(a) large (1);
(b) small (2); and
(c) not visible (3).

b

c

as follows for statistical processing: 1 = not difficult (10–16 points), 2 = average difficulty (17–
23 points) and 3 = difficult (24–30 points). The
data were processed using the SPSS statistical
package (IBM SPSS Statistics for Windows, Version 21.0, IBM, Armonk, N.Y., U.S.). Normal distribution of the variables was evaluated by the
Kolmogorov–Smirnov test and was conﬁrmed in
all cases. Multivariate analysis was performed,
involving the estimation of a general linear multiple regression model for the selected response
variable (time) as a function of the study param54 Volume 3 | Issue 1/2017

eters and surgical difficulty scores. The accepted
level of statistical signiﬁcance was 5% (ʸ = 0.05).

Results
One hundred patients (41 men and 59 women)
between 18 and 45 years of age (mean age of
24.9 ± 6.5 years) were analyzed. Mandibular left
(n = 49) and right (n = 51) third molars were extracted. The maximum ﬁnal score was 27 points,
with a minimum ﬁnal score of 13 (mean ﬁnal

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Evaluation of surgical difficulty of extraction

Figs. 4a–c

a

b

c

Figs. 5a–c

a

b

a

b

c

Figs. 6a–c

c

score of 19.4 ± 2.6 points). Extraction was not
difficult in 14.6% of the patients (10–16 points
on the surgical difficulty scale), of average difficulty in 79.2% (17–23 points) and difficult in
6.3% (24–30 points).
The maximum ostectomy time was 180 s, with
a minimum time of 10 s (mean of 54.4 ± 28.2 s).
Tooth sectioning was carried out in 74 cases, with a
mean duration of 73.4 ± 45.7 s (maximum of 284 s).
The mean total surgical time was 10.8 ± 5.3 min
(maximum of 30 min and minimum of 4 min).
The mean total surgical time was signiﬁcantly
longer in the case of molars with mesial inclination and in distal or horizontal presentations
(p = 0.043). There were no great differences on
comparing inclination of the second molar and
pericoronal and root radiolucency. However, very
signiﬁcant differences were observed on com-

paring root shape with ostectomy time (p = 0.001)
and total surgical time (p = 0.001; Table 1).
The general linear multiple regression model
showed the quantitative parameters with the
greatest influence upon ostectomy time to be
Winter’s distance and the distance from the ascending ramus to the second molar. A greater
Winter’s distance prolonged ostectomy time and,
conversely, a greater distance from the mandibular
ramus to the distal surface of the second molar
was observed to shorten ostectomy time. The
parameters found to be linearly correlated to total
surgical time were coronal width and the distance
from the ramus to the second molar. Total surgical
time was longer in the presence of greater coronal
width and a shorter distance from the ramus to
the second molar. The only variable correlated to
tooth sectioning time was coronal width (Table 2).

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Figs. 4a–c
Root radiolucency:
(a) large (1);
(b) small (2); and
(c) not visible (3).
Figs. 5a–c
Root shape:
(a) single or fused (1);
(b) separate (2); and
(c) dysmorphic or
anomalous (3).
Figs. 6a–c
Winter’s distance:
(a) < 5 mm (1);
(b) 5–9 mm (2); and
(c) > 9 mm (3).

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Evaluation of surgical difficulty of extraction

Figs. 7a–c

c
Figs. 8a–c

Figs. 7a–c
Coronal width:
(a) < 10.0 mm (1);
(b) 10.0–11.5 mm (2); and
(c) > 11.5 mm (3).
Fig. 8a–c
Distance from mandibular
ramus to distal surface of the
second molar:
(a) 10.5–14 mm (1);
(b) 8.0–10.5 mm (2); and
(c) 2.0–8.0 mm (3).

According to the model, higher scores on the
radiographic scale were associated with longer
ostectomy time and total surgical time. For each
additional point increase on the scale, the
ostectomy time was seen to increase by 2.89 s,
while the total surgical time increased by 0.56 s.

Discussion
In order to successfully predict the difficulty of
impacted mandibular third molar extraction,
consideration is required of the clinical and radiographic ﬁndings, which not only help to plan
surgery, but also to increase patient satisfaction
with the treatment received. Barreiro-Torres et
al. underscored the importance of operator
expertise in establishing a prior diagnosis of surgical difficulty, since an expert dental professional tends to underestimate surgery and only
examine the radiographs—and this in turn can
lead to a failed estimation of extraction difficulty.8
The various systems developed for estimating surgical difficulty in extracting impacted
mandibular third molars are based on preoper56 Volume 3 | Issue 1/2017

ative examination of the panoramic radiographs.
Although the classiﬁcations of Pell and Gregory1
and Winter2 have served as references, some
authors, such as García-García et al.,9 have found
the classiﬁcation of Pell and Gregory to offer
low sensitivity: It failed to detect many of those
cases that subsequently proved to be very difﬁcult when classiﬁed with the scale of Parant.10
This scale,10 in contrast to the presurgical radiographic scale used in the present study, was
designed to assess the difficulty of extraction
from the clinical perspective: It is based on the
need for rating from greater to lesser surgical
effort, but lacks predictive value. Pedersen3
added a further factor to the classiﬁcation of
Pell and Gregory1—the position of the third
molar—and predicted surgical difficulty from the
sum of the individual scores of the scale.
With the aim of establishing a preoperative
diagnosis of surgical difficulty, various investigators have proposed scales based on a series
of clinical and radiographic parameters. Peñarrocha et al. added the variables of inclination of
the third molar and inclination of the second
molar, pericoronal radiolucency, pericoronal
space, Winter’s distance, length and type of root,

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Evaluation of surgical difficulty of extraction

Figs. 9a–c

a

b

c

Figs. 10a–c

a

b

c

and coronal area to the classical variables of Pell
and Gregory,1 producing the predictive scale with
the largest number of variables to date, and adding ostectomy time as an indicator of surgical
difficulty.5 These authors recorded longer ostectomy times in those cases predicted to be the
most difficult extractions according to their classiﬁcation.5 This is consistent with the ﬁndings
of the present study, in which the variables mesiodistal diameter of the third molar and root
radiolucency were added to the classiﬁcation of
Peñarrocha et al.,5 and ostectomy time, tooth
sectioning time and total surgical time were also
considered.
The relationship between the difficulty of
extraction and the parameters evaluated by the
various presurgical scales is usually appraised
on the basis of the total surgical time. The results
obtained in the present study point to a linear
relationship between the surgical difficulty score
and the total surgical time and ostectomy time.
Santamaría and Arteagoitia demonstrated a relationship between the difficulty of extraction
and the depth of impaction, the width of the
periodontal ligament, the inclination of the third
molar, its relation to the second molar, and the

distance between the mandibular ramus and the
second molar.11 According to Yuasa et al., the most
important variables for assessing the difficulty of
mandibular third molar extraction are depth
level C, Class 3 and large roots, or the combination
of these three factors—all of which can be recorded from the panoramic radiographs.12 López
Arranz underscored the importance of evaluating
the adjacent teeth: The presence of the ﬁrst and
second molars, their anatomical integrity and
separate roots constitute important support for
extraction of the third molar.13
In the present study, the mesiodistal diameter of the third molar and the distance
between the mandibular ramus and the second
molar were the parameters most closely correlated to total surgical time. This was in contrast to Carvalho and do Egito Vasconcelos, who
identiﬁed the number of roots and their morphology, the position of the tooth, the periodontal
space, and the relation to the second molar as
the only signiﬁcant predictors.14 These authors
associated the greatest surgical difficulty with
Class 3 cases on the scale of Pell and Gregory.1
The observations of Yuasa et al.12 and those of
the present study indicate that long distances

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Figs. 9a–c
Coronal area:
(a) 20–75 mm2 (1);
(b) 75–90 mm2 (2); and
(c) 90–130 mm2 (3).
Figs. 10a–c
Root length:
(a) 3.0–8.0 mm (1);
(b) 8.0–9.5 mm (2); and
(c) 9.5–13.0 mm (3).

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Table 1

Mean ostectomy time by
group (seconds)

Variable

Group

Inclination of third molar

Vertical (1)
Mesial (2)
Distal or horizontal (3)

47.7
51.1
63.3

Inclination of second molar

Mesial (1)
Vertical (2)
Distal (3)

54.1
54.5
53.5

Pericoronal radiolucency

Large (1)
Small (2)
Not visible (3)

48.1
58.0
51.7

Root radiolucency

Large (1)
Small (2)
Not visible (3)

52.9
54.4
56.0

Root shape

Single or fused (1)
Separate (2)
Dysmorphic or anomalous (3)

39.4
47.9
67.6

Mean total surgical time
(minutes)

p = 0.141

8.7
10.2
12.9

p = 0.043*

p = 0.996

10.9
10.7
9.0

p = 0.886

p = 0.295

10.6
10.7
10.9

p = 0.993

p = 0.939

10.1
11.0
10.9

p = 0.732

p = 0.001*

8.1
9.5
13.1

p = 0.001*
*p < 0,05; **p < 0,01
Table 2

Ostectomy time

Tooth sectioning time

Total surgical time

p-value (r)

p-value (r)

p-value (r)

Winter’s distance

0.025* (r = 0.232)

0.928 (r = -0.011)

0.406 (r = 0.087)

Coronal width

0.687 (r = -0.042)

0.006** (r = 0.317)

0.007** (r = 0.276)

Distance from mandibular
ramus to distal surface of
second molar

0.009* (r = -0.270)

0.144 (r = -0.172)

0.027* (r = -0.230)

Coronal area

0.143 (r = -0.154)

0.358 (r = 0.109)

0.838 (r = -0.022)

Root length

0.470 (r = -0.077)

0.324 (r = 0.118)

0.157 (r = 0.150)
*p < 0,05; **p < 0,01

Table 1
Study parameters with
the greatest inﬂuence upon
surgical difficulty.
Table 2
Correlation of the quantitative
parameters to the variable
time according to the general
linear multiple regression
model.

between the ascending mandibular ramus and total surgical time. The strongest predictors of
the distal surface of the second molar (Class 3) ostectomy time were Winter’s distance, the distance from the mandibular ramus to the second
shorten the surgical time.
molar, and root shape, while the strongest predictor of tooth sectioning time was coronal
Conclusion
width. The parameters that influenced total
surgical time the most were coronal width,
In summary, an analysis of the surgical difficulty mesial and distal or horizontal inclination of the
of impacted mandibular third molar extraction is third molar, separate and dysmorphic or anomessential for treatment planning and helps assess alous roots, and the distance between the manprofessional surgical skill, reduces complications, dibular ramus and the second molar.
optimizes patient preparation, and minimizes
postoperative pain and inﬂammation.
Competing interests
Our scale is effective, since the mandibular
third molars with the highest scores were signi- The authors declare that they have no competﬁcantly correlated to longer ostectomy time and ing interests.
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References
1.
Pell G. Gregory B. Impacted mandibular
third molars: classiﬁcation and modiﬁed
techniques for removal.
→ Dent Dig.
1993;39:330–8.
2.
Winter GB. Principles of exodontia as
applied to the impacted third molar.
→ St Louis: American Medical Book Co;
1926. p.21-58.
3.
Pederson GW. Oral surgery. Philadelphia:
WB Saunders, 1988 (Cited in: Koerner KR.
The removal of impacted third molarsprinciples and procedures.
→ Dent Clin North Am.
1994;38:255-78).
4.
Cáceres Madroño E, Martinez-González
JM, Meníz García C, López Carriches C,
Madrigal Martínez-Pereda C. Estudio del
grado de diﬁcultad en la extracción de
los terceros molares inferiores en relación
con la experiencia profesional; Periodo
preoperatorio (Parte I).
→ Arch Odontoestomatol.
1998;14(4):229–37.

5.
Peñarrocha M, Sanchis JM, Sáez U,
Gay Escoda C, Bagán JV. Escala numérica
de valoración de la diﬁcultad quirúrgica
en la extracción de 190 terceros molares
mandibulares incluidos.
→ Arch Odontoestomatol.
2000;16(2):96–100.
6.
Romero Ruiz MM. El tercer molar incluido.
→ In: Romero Ruiz MM, Gutiérrez Pérez JL,
editors. El tercer molar incluido. Madrid:
GSK;
2001. p. 43–69.
7.
Schneider, C. A.; Rasband, W. S. & Eliceiri,
K. W. (2012), "", Nature methods 9(7):
671-675
8.
Barreiro-Torres J, Diniz-Freitas M,
Lago-Méndez L, Gude-Sampedro F,
Gándara-Rey JM, García-García A.
Evaluation of the surgical difficulty in lower
third molar extraction.
→ Med Oral Patol Oral Cir Bucal.
2010 Nov 1;15(6):e869–74.

9.
García-García A, Gude-Sampedro J,
Gándara-Rey JM, Gándara-Vila P,
Somoza-Martin M. Pell-Gregory
classiﬁcation is unreliable as a predictor
of difficulty in extracting impacted lower
third molars.
→ Br J Oral Maxillofac Surg.
2000 Dec;38(6):585–7.
10.
Parant M. Petite Chirurgie de la Bouche.
Paris: Expansion Cientiﬁque, 1974.
(Cited in: García GA. Sampedro GF, Rey GJ,
Torreira GM. Trismus and pain after
removal of impacted lower third molars.)
→ J Oral Maxillofac Surg.
1997;55:1223-6.

13.
López Arranz JS. Diagnóstico por la
imagen.
→ In: López Arranz JS, editor. Cirugía oral.
Madrid: Interamericana-McGraw-Hill.
1991. p. 65–118.
14.
Carvalho RW, do Egito Vasconcelos BC.
Assessment of factors associated
with surgical difficulty during removal of
impacted lower third molars.
→ J Oral Maxillofac Surg.
2011 Nov;69(11):2714–21.

11.
Santamaría J, Arteagoitia I. Radiologic
variables of clinical signiﬁcance in the
extraction of impacted mandibular third
molars.
→ Oral Surg Oral Med Oral Pathol Radiol
Endod.
1997 Nov;84(5):469–73.
12.
Yuasa H, Kawai T, Sugiura M. Classiﬁcation
of surgical difficulty in extracting impacted
third molars.
→ Br J Oral Maxillofac Surg.
2002 Feb;40(1):26–31.

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Kinesiographic analysis

Kinesiographic analysis of lateral
excursive movement on the horizontal
plane: the retrusive component
Abstract
Objective
Andrea Papini,a Gianfranco Cesarettib
& Patrizia De Fabianisc
a

Private practice in Prato, Italy
ARDEC Academy, Rimini, Italy
c
Turin University, Turin, Italy
b

Corresponding author:
Dr. Gianfranco Cesaretti
Via Maria Montessori 9
60022 Castelﬁdardo AN
Italy
T +39 071 782 2800
giancesa55@gmail.com

The temporomandibular joint (TMJ) has a functionally complex articulation
that during phylogeny underwent an adaptation also linked to posture
change after the acquisition of upright posture and subsequent reduction
of the postglenoid process. This articulation supports numerous functions
of the stomatognathic apparatus, and the part physiologically designed to
withstand greater loads associated with mastication is essentially the
frontal one; the rear portion of the TMJ is unﬁt to absorb retrusive forces
owing to the poor support of the thin bone component and the histological
characteristics of the tissue component. The purpose of this article was
to analyze the angles of lateral tracings both on the frontal plane and on
the horizontal one through kinesiographic analysis (functional masticatory angle of Planas and functional horizontal masticatory angle) in seeking
to observe their mutual relations with respect to those planes.
Materials and methods

How to cite this article:
Papini A, Cesaretti G, De Fabianis P. Kinesiographic analysis
of lateral excursive movement on the horizontal plane:
the retrusive component.
J Oral Science Rehabilitation.
2017 Mar;3(1):60–7.

The study was performed on 115 patients who presented with asymmetrical laterality movements. The sample was made up of 32 males and 85
females aged between 17 and 84.
Results

Ninety-eight (85%) of the lateral tracings examined showed a consistency between the inclination of the tracings on the frontal and horizontal
planes. Seventeen (15%) showed an inconsistency between the inclination of the tracings on the horizontal and frontal planes.
Conclusion

The study found a correspondence on the working side between a steep
laterality on the frontal plane and a posterior trajectory on the horizontal
plane. The reduction of the steepness of the functional masticatory angle
of Planas tends to reduce the posteriorization of the functional horizontal masticatory angle, promoting the recovery of alternating unilateral
masticatory function.
Keywords

Temporomandibular joint (TMJ), Gothic arch, functional masticatory
angle of Planas (AFMP), functional horizontal masticatory angle (AFMO),
masticatory cycle, lateral retrusion Posselt volume.
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Introduction
The phylogenetic evolution has produced a number of postural changes related to the attainment
of the upright position, and the TMJ, in its relationship to the tympanic cavity, has undergone a
transformation. In fact, while both in anthropomorphic and in nonanthropomorphic monkeys,
the rear portion of the TMJ is bounded posteriorly by the postglenoid process1—a bony protuberance of marked thickness that delimits and
separates the mandibular fossa from the tympanic cavity2—in Homo sapiens, this process has
had a progressive thinning, ending in a factual
disappearance. Therefore, in modern man, the
rear wall of the mandibular fossa forms the front
wall of the tympanic cavity. It is a thin layer,
crossed by a canal (named Huguier’s or Civinini’s
canal, after the researcher who ﬁrst described it)
that connects the two structures.3, 4 The softtissue that makes up the retrodiscal portion of
the TMJ is histologically unﬁt to withstand compressive forces, as the retrodiscal portion of the
TMJ, richly vascularized and innervated,5 essentially acts as a hydrodynamic support. It is worth
considering that some of the connective ﬁbers of
the retrodiscal tissue penetrate the Huguier’s
canal,6 forming the discomallear ligament and
reaching the tympanic cavity, attaching to the
malleus head and neck. In summary, these characteristics make the posterior region of the TMJ
unsuitable for bearing the functional loads of
mastication and swallowing, since, under optimum conditions, the condyle should never cause
excessive compression of retrodiscal tissue. In
fact, prolonged and constant compressive stress,
linked for instance to dysfunctional situations,
determines stresses that tend over time to result
in reparative fibrotic processes,7, 8 leading to
structural changes9, 10 responsible for a different
biomechanical response of the tissue.
The study of mandibular movement on the
horizontal plane is associated with the interincisal point movement. Gysi in his records11 was
the ﬁrst to describe the Gothic arch: In classic
gnathology the lateral tracings on the horizontal
plane are described as an anterolateral shift.
Symmetrical on both sides, the lateral tracings
on the frontal plane are usually described as an
anterolateral development. In patients with dysfunction, kinesiographs show as a norm a deformation of the Gothic arch: One of the two lateral tracings tends to lose the anterolateral
direction to acquire a tendency to posteriorization (Fig. 1). Guichet has described a 60° conic

volume in which the working condyle can shift
during the lateral excursion.12 The interincisal
point used in the recording of the Gothic arch
can be placed geometrically in relation to the
condyles.13, 14 Mongini has described in the position of maximum intercuspation the relationships between the interincisal point and the
position of the condyles.15
Through the aid of a kinesiograph during lateral excursion, the tracing of the interincisal
point on the horizontal plane can be placed in
relation to the movement of the working condyle: during lateral excursion, the balancing
condyle always shifts in the anteromedial direction, while the working condyle can move both
in the anterolateral direction and in the posterolateral one. The interincisal point will have the
same tendency of the working condyle movement (Fig. 2). The Gothic arch, which highlights
the excursive interincisal movements of the
point on the horizontal plane, can be considered
a horizontal section of a volume defined by
Posselt with the trajectories of maximum movements of opening, laterality and protrusion.16
The volume of Posselt can be deﬁned as a 3-D
perimeter within which the jaw can achieve its
functional movements.
In patients with dysfunction, an asymmetrical Gothic arch, altered and reduced in its developments, is practically the norm and must be
interpreted as a planar representation of the
deformation of the entire Posselt volume (Fig. 3).
Alternating unilateral mastication allows better
control of the food bolus and of the forces that
develop during mastication; from a biomechanical point of view, it tends to symmetrically allocate the distribution of load on the dental, periodontal, bone, joint and muscle structures. This
alternation of the masticatory cycles is permitted by the symmetry of the functional masticatory angles of Planas (AFMP, angles fonctionnels
masticatoires de Planas). The AFMPs are the
angles that are created on the frontal plane
between the lateral distances and the horizontal
plane, while the functional horizontal masticatory angles (AFMO) are those that are created
on the horizontal plane between the lateral distances and the frontal plane (Fig. 4). In the presence of a retrusive AFMO, there will be a deformation of the Gothic arch structure (Fig. 1).
The purpose of this work was to analyze the
angles of lateral tracings, seeking to observe the
relation of coherence between the frontal plane
and the horizontal plane (AFMP/AFMO). This
consistency respects the correspondence

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Fig. 1

Fig. 1
Kinesiographic tracings:
dysfunctional Gothic arches.

Fig. 2

Fig. 2
Relation between the
interincisal point movement
and the working condyle
movement.

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Fig. 3

Fig. 3
Posselt diagrams in patients
with dysfunction.
Fig. 4
Frontal plane: AFMP.
Horizontal plane: AFMO.

Fig. 4

between the front slope of the AFMP and plane, and the magnet was placed in an equidisanteroposteriority of the AFMO.
tant position with respect to the two detectors
of the kinesiograph.
Materials and methods
Results
The study was performed on 115 patients who
presented with asymmetrical lateral excursion
The sample was made up of 32 males and 85
females aged between 17 and 84. The instrument used for this study was a Bioket kinesiograph (Bioket, S.Benedetto del Tronto, Italy).
Eligible subjects were placed in a sitting position,
not on the dental chair, feet with full plantar
support on the ﬂoor. The kinesiographic mask
was positioned with reference to the horizontal

Ninety-eight (85%) of the lateral tracings
examined with respect to the frontal plane
showed consistent results, demonstrating the
correspondence between the greater steepness
of the AFMP and the posteriorization of the
AFMO. The steepest laterality in the frontal
plane was found to be the most posterior on the
horizontal plane. The remaining 17 (15%) tracings
failed to show this kind of correspondence

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Fig. 5
Correspondence between
a steep AFMP and a retrusive
AFMO
(always found to be < 1).

Fig. 5

Fig. 6
Asymmetric lateral excursion.

Fig. 6

between the AFMP and the AFMO. On the
horizontal plane, the lateral retrusion formed an
angle with the frontal plane that was given a
negative value, and the angles formed by lateroprotrusive tracings were given a positive value.
On the horizontal plane in all of the 98 coherent
paths, the relationship between the angle of the
tracing corresponding to that steeper on the
frontal plane and that corresponding to the less
steep was always found to be < 1, showing the
correspondence between a steep AFMP and a
retrusive AFMO (Fig. 5). The average conﬁrmed
precisely precisely the correspondence between
a steep AFMP and a retrusive AFMO:
A1/B1 = - 0.589432199.
64 Volume 3 | Issue 1/2017

Discussion and conclusion
Planas in deﬁning the AFMP emphasized the
pattern of unilateral mastication.17 Predominantly
unilateral mastication usually occurs when there
is a side of the mouth in which the function can
be performed with more ease and efficiency
compared with the contralateral side (Fig. 6).
Predominantly unilateral mastication tends to
develop from the side with less steep laterality
or with a smaller AFMP. The study of laterality
with a Bioket kinesiograph has permitted to
highlight also on the horizontal plane the asymmetry deﬁned by Planas on the frontal plane:
On the horizontal plane, the side with the less

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Fig. 7
Frontal plane: masticatory
cycles in predominantly
unilateral mastication on the
side with the less steep AFMP.
Horizontal plane: masticatory
cycles in predominantly
unilateral mastication on the
side with the advanced AFMO.

Fig. 7

Fig. 8
Unilateral masticatory cycles.

Fig. 8

steep AFMP (usually the one with an easy lateral excursion and functionally prevailing masticatory side) tends to correspond to the side
with the tracing that is expressed in anteriority
(Fig. 7) and vice versa. This is referred to as the
consistency of the tracings of laterality between
the front and the horizontal planes.
An AFMO tending to posteriorization is an
index of laterality with a retrusive component:
The entry stage of the masticatory cycle (during
which the masticatory forces reach their maximum intensity) tends to take place with an unfavorable condyle–fossa relationship. A lateral
retrusion tends to create a compression of the
retrodiscal tissue, hindering proper mastication

and encouraging mastication on the contralateral side (Fig. 8).
By decreasing the steeper slope and the lateral tracings symmetrizing the AFMP on the
frontal plane, the retrusion of the corresponding
AFMO tended to reduce, resulting in a regularization of the Gothic arch and of the Posselt
volume and favoring the restoration of alternating unilateral mastication (Fig. 9). Since the
tracing of the Gothic arch is a horizontal section
of the Posselt volume, the arch regularization
determines a volume regularization that allows
the jaw to move freely in mastication (Fig. 9).
Therefore, analysis of lateral excursion
movements with evaluation of the prevailing

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Fig. 9

Figs. 10a & b

Fig. 9
Decreasing the AFMP on the
frontal plane tended to
reduce the retrusion of the
corresponding AFMO on
the horizontal plane,
correcting and regularizing
the Posselt volume.
Figs. 10a & b
Bonwill’s triangle.

masticatory side cannot exclude analysis of lateral excursion on the horizontal plane. In kinesiographic tracings of patients with dysfunction,
the asymmetries of the AFMP and AFMO (and
therefore of the Gothic arch and the Posselt
volume) are largely the norm: Steeper laterality
on the frontal plane will tend to have a retrusive
tracing (absolute or relative to the contralateral
side) on the horizontal plane.
The back thrust of the working condyle in
lateral retrusive tracings of will tend to be
– directly proportional to the posteriorization of
the interincisal tracing;
– directly proportional to the length of the
tracing—the more the lateral tracing has to
express its posterior movement, the more the
working condyle will tend to posteriorization
(Fig. 10a);
– inversely proportional to the vertical component of the movement: because the lateral
excursion is expressed on the different spatial
planes, the vertical component is as if it
tended to stop the retrusive push of the working condyle (Fig. 10b).

steeper inclination of the AFMP will tend to
reduce the retrusion of the corresponding
AFMO, regularizing the Gothic arch and the
Posselt volume, and this will promote the restoration of alternating unilateral mastication.
Acting properly on the occlusal surfaces, we
are able to inﬂuence the whole of the mandibular
dynamics by changing not only the movements
related to occlusal guides, but also the mandibular movements in full, both in the amount of
maximum openness, in their transverse width
and in their inclination. Premature contacts or
interferences that induce retrusion of the
lateral excursion on the horizontal plane with
posteriorization of the entry phase of the masticatory cycle will tend to favor prevalent mastication on the contralateral side. With asymmetry correction of lateral excursion, we tend to
decrease the condylar retrusion, expand and
symmetrize the Gothic arch and the volume
of Posselt, thus directing the masticatory function to a physiological alternating unilateral
mastication.

Competing interests
A posterior AFMO (absolute or relative to the
contralateral side) indicates a difficult, countered The authors declare that they have no conﬂict
laterality and will tend to highlight the side with of interest regarding the materials used in the
problematic masticatory function. Reducing the present study.
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Physiological bone remodeling on Osstem implants

Open-cohort prospective study on early implant
failure and physiological marginal remodeling
expected using sandblasted and acid-etched bone
level implants featuring an 11° Morse taper connection
within one year after loading
Abstract
Objective
Marco Tallaricoa & Silvio Mario Melonib
a

Aldent University, Tirana, Albania; private practice,
Rome, Italy
b
University of Sassari, Sassari, Italy; private practice,
Arzachena, Italy

Corresponding author:
Dr. Marco Tallarico
Via di Val Tellina 116
00151 Rome
Italy
T +39 06 663 0646
me@studiomarcotallarico.it

The objective of this study was to evaluate the implant survival and success
rates as well as the physiological marginal bone remodeling expected
using Osstem implants.
Materials and methods

This investigation was designed as an open-cohort prospective study on
completely or partially edentulous patients who received at least one bone
level implant with a sandblasted and acid-etched surface and an 11° Morse
taper connection. Outcome measures were the success rates of the implants and prostheses, complications, marginal bone level changes, insertion torque, implant stability quotient, bone density and soft-tissue
biotype.
Results

How to cite this article:
Tallarico M, Meloni SM. Open-cohort prospective study
on early implant failure and physiological marginal
remodeling expected using sandblasted and acid-etched
bone level implants featuring an 11° Morse
taper connection within one year after loading.
J Oral Science Rehabilitation.
2017 Mar;3(1):68–79.

A total of 243 implants were placed in 90 consecutive patients and followed up for a minimum period of one year after loading (mean of
17.6 ± 2.5 months; range of 12–24 months). Five implants failed in ﬁve
patients, resulting in a cumulative implant survival rate of 97.9%. Insertion
torque of < 35 N cm was found to be a risk factor for implant failure
(p = 0.0068). No deﬁnitive prosthesis failed, resulting in a cumulative
prosthetic survival rate of 100%. Four patients experienced one technical
complication each, resulting in a cumulative prosthetic success rate of
97.2%. The cumulative mean marginal bone loss between implant placement and the follow-up one year after loading was 0.37 ± 0.25 mm (95%
CI: 0.26–0.30). Comparison of marginal bone loss and the investigated
risk factors found statistically higher marginal bone loss for smokers, a
thin gingival biotype and guided bone regeneration (p < 0.05).
Conclusion

Low implant failure and physiological marginal bone remodeling of
0.37 mm within one year after loading can be expected using Osstem TSIII
implants in the daily practice.
Keywords

Dental implants, bone remodeling, conical connection, survival
rate, complications.
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Introduction
During the first year of function, a certain
amount of physiological marginal bone loss
is expected around a dental implant, both
horizontally and vertically; thereafter, minimal further bone loss has been observed.1, 2
Marginal bone loss (MBL) of 1.5–2.0 mm during
the ﬁrst year of function has been assumed as
normal. 2 Afterward tissue stability is expected.2–4 However, the criteria for deﬁning success
in implant dentistry are under constant debate
in consensus statements and observational
studies. Papaspyridakos et al. proposed parameters related to soft- and hard-tissue stability
that can influence the progression of MBL
around implants, but is not clear whether the
physiological bone remodeling is prosthesis-related, host-related, implant-related or loaddependent.4 As a result, although numerous
studies have reported improvements in implant
design and protocols to minimize this MBL, the
utilized criteria for success have remained
unchanged.
Several factors may increase MBL around
dental implants, including surgical trauma,
implant–abutment connection type, biological
width establishment, mucosal tissue thickness,
keratinized tissue width and bone density.5–7 The
stress and strain concentrated at the periimplant
crestal bone result in structural and morphological changes, especially during the ﬁrst year
after loading.7 Hence, the bone remodeling process is one of the critical factors in evaluating
implant success.8 In addition, iatrogenic factors
may contribute to periimplant MBL, such as implant positioning, implant–abutment microgap,
lack of passive ﬁt of the superstructure and occlusal overloading.9–13
Many pathological factors, including history
of periodontitis, smoking, poor plaque control,
genetic predisposition and diabetes, may produce an inflammatory reaction around an
implant; nevertheless, no consensus exists with
regard to a suitable deﬁnition of “periimplantitis”
based on clinical and radiographic signs and
symptoms or the best way to manage this
emerging challenge.13, 14 The American Academy
of Periodontology in 2013 deﬁned “periimplantitis” as an inﬂammatory reaction associated
with the loss of supporting bone beyond the
initial biological bone remodeling around an implant in function.15
The aims of the present study were to report
the survival and success rates of dental implants

placed in private practice and representing the
daily realities of implant treatment, and then to
determine the entity of the physiological marginal bone remodeling expected using Osstem
implants. The data were analyzed to determine
any statistical relationships between explanatory variables and early implant failure and
physiological marginal bone remodeling (within
one year after loading). This study is reported
according to the Strengthening the Reporting of
Observational Studies in Epidemiology statement for improving the quality of observational
studies.16

Materials and methods
This investigation was designed as an opencohort prospective study. All of the surgical and
prosthetic procedures were performed in a private center in Rome, Italy, by an implant-based
certified clinician (MT) between September
2014 and December 2016. All of the participants
were enrolled and treated in consecutive order
after being informed about the clinical procedures, materials to be used, beneﬁts, and potential risks and complications, and once their written consent had been obtained. This study was
conducted according to the principles embodied
in the Helsinki Declaration of 1975, as revised in
2008.
Any completely or partially edentulous
patients who received at least one bone level
implant with a sandblasted and acid-etched surface and a Morse taper connection (Osstem
TSIII, Osstem, Seoul, South Korea) were considered eligible for this study, independent of the
implant and prosthetic protocols used. Exclusion
criteria were general medical contraindications
to oral surgery (American Society of Anesthesiologists Physical Status Class III or IV), patients
treated or under treatment with intravenous
aminobisphosphonates, and previous radiotherapy of the oral and maxillofacial region
within the last ﬁve years. Patients who were
diagnosed with active periodontal disease
(≥ 6 mm probing depth) underwent periodontal
surgery or initial therapy alone, prior to implant
surgery.
Surgical and
prosthetic protocols

Preoperative photographs, periapical radiographs, panoramic radiographs or cone beam

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computed tomography (CBCT) scans, and model
casts were produced for all of the patients, for
initial screening and case evaluation. Before
implant placement, all of the patients received
a single dose of an antibiotic (2 g of amoxicillin
or 600 mg of clindamycin if allergic to penicillin).
Prior to the start of surgery, the patients rinsed
with 0.2% chlorhexidine for 1 min. The patients
received Osstem TSIII bone level implants with
a rough surface (Ra of 2.5~3.0 μm) sandblasted
with alumina and acid-etched and featuring an
internal hex and 11° conical connection. Implant
placement was performed using either computer-guided template-assisted implant placement
or conventional freehand surgery. Most of the
implants were placed according to the drilling
protocol recommended by the manufacturer. In
the case of immediate loading, post-extractive
implants and poor bone quality, the drilling protocol was customized (Table 1).
Surgical protocols included placement in
completely or partially edentulous healed ridges
with or without bone grafting, as well as in fresh
extraction sockets using a ﬂapless or a ﬂap approach. A ﬂapless approach was planned in the
case of post-extractive implants or in a healed
site, depending on the width of the available
keratinized mucosa. In cases of ridge atrophy,
deﬁned as a bone height of < 7.0 mm and/or bone
width of < 4.5 mm, implant placement was performed simultaneously with guided bone regeneration (GBR). Otherwise, in cases of severe
ridge atrophy, implant placement was performed six months after bone regeneration.
Sinus lift procedures were performed using the
conventional lateral window technique or by a
less invasive transcrestal sinus ﬂoor elevation
(Crestal Approach Sinus KIT, CAS-KIT, Osstem)
in the case of a residual alveolar crest of at least
3 mm (maximum of 8 mm) in height and 6 mm
in width distal to the canine, measured on a
CBCT scan. In all reconstructive cases, the bone
graft material was based on autogenous bone,
combined with synthetic hydroxyapatite enriched with magnesium (SINTlife, Finceramica,
Faenza, Italy) or with beta-tricalcium phosphate
(Q-Oss+, Osstem). A resorbable cross-linked
collagen membrane (OssGuide, Osstem) was
used to protect the graft material during healing
in the case of GBR or the lateral window approach.
In the case of immediate post-extractive implants, residual teeth were extracted as atraumatically as possible. Implant insertion was then
planned along the palatal socket wall, about
70 Volume 3 | Issue 1/2017

1.5 mm below the buccal alveolar crest. The
residual socket was grafted with corticocancellous heterologous bone, with a graft particle size
of 250–1,000 μm (OsteoBiol Gen-Os, Tecnoss,
Giaveno, Italy). In the case of delayed implants,
socket preservation was performed with the
same procedure and the implant was placed four
months after healing.
Loading protocols varied based on implant
stability and/or individual case requirements.
Immediate loading (within 48 h of implant placement) was performed in the case of an implant
stability of at least 35 N cm and at the patient’s
request. Titanium temporary abutments or
titanium or zirconia deﬁnitive abutments were
screwed directly on to the implants or the intermediate abutments (straight or angulated
multi-abutments, Osstem) with prosthetic
screws tightened to 15 N cm on the day of
surgery. Straight or angled multi-abutments
(Osstem) were used in the case of multiunit restorations and screw-retained prostheses and/or
when there was the need to change the depth or
the angle of the implant. Prefabricated, screw-retained or cemented temporary acrylic restorations were trimmed and polished chairside.
Partially edentulous patients received nonocclusal temporary restorations. Multiple implants
received splinted, metal-reinforced temporary
restorations with centric contact and group function, but without any cantilever. If needed, ﬂaps
were closed around the abutments. Otherwise,
in the case of a bone augmentation procedure or
post-extractive implants, a conventional or delayed loading protocol (three to six months after
implant placement) was adopted.17
After implant placement, all of the patients
received oral and written recommendations on
medication, oral hygiene maintenance and diet.
Postoperative antibiotic therapy (1 g of amoxicillin or 300 mg of clindamycin), administered
every 12 h for six days, was limited to cases with
immediate socket sites, bone grafting or sinus
procedures. Analgesics (500 mg of paracetamol
plus 30 mg of codeine, or 600 mg of ibuprofen)
were administered as needed.
Final restorations were delivered between
eight (single or partial crowns and overdentures)
and twenty weeks (full arches). Final restorations were either screw-retained or cemented.
Cemented restorations were delivered on either
stock or customized CAD/CAM abutments. All
of the restorations (metal and zirconia) were
cemented using a glass ionomer cement (Ketac
Cem, 3M ESPE, Neuss, Germany). Any cement

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Physiological bone remodeling on Osstem implants

Table 1

Type

Subtype

Implant protocol and location

Conventional preparation

Healed site

Adapted preparation technique

Narrow preparation

Freehand, maxilla required
immediate loading, post-extractive
implants, poor bone quality

Halfway preparation

Guided surgery, maxilla,
immediate loading

Osteotome technique

Maxilla, needed to perform
bone spreading

remnant was immediately removed using an
air–water syringe with the patient’s mouth
closed. After 5 min of setting, the patient was
clinically and radiographically inspected. Otherwise, CAD/CAM screw-retained restorations
were delivered at implant or abutment level. The
ﬁnal abutments and screw-retained frameworks
were screwed on at the torque setting recommended by the manufacturer.
The patients that received cemented restorations were inspected again after three to ﬁve
days. All of the patients were then enrolled in a
standard implant recall program. Oral hygiene
maintenance was checked and radiographs were
taken early after ﬁnal prosthesis delivery. Occlusion was checked at every appointment. An
explanatory case is illustrated in Figures 1 to 10.
Outcomes

Primary outcome measures were the success
rates of the implants and prostheses, evaluated
by an independent assessor. An implant was considered a failure if it presented any mobility, assessed by tapping or rocking the implant head
with the metallic handles of two instruments,
progressive MBL or infection, and any mechanical
complications rendering the implant unusable,
although still mechanically stable in the bone. A
prosthesis was considered a failure if it needed
to be replaced with another prosthesis.
Secondary outcomes were as follows:
– Complications: Any biological (pain, swelling,
suppuration, etc.) and/or mechanical (screw
loosening, fracture of the framework and/or the
veneering material, etc.) complications were
evaluated and treated by the same surgeon.
– Marginal bone levels: The levels were assessed
using intraoral digital periapical radiographs

(Digora Optime, SOREDEX, Tuusula, Finland;
photostimulable phosphor imaging plate, size
2, pixel size of 30 μm, resolution of 17 lp/mm)
at the subsequent follow-ups: implant placement (baseline), second-stage surgery, deﬁnitive crown delivery and one year after loading.
Intraoral radiographs were taken with the
paralleling technique by means of a periapical
radiograph with a commercially available ﬁlm
holder (Rinn XCP, Dentsply Rinn, Elgin, Ill.,
U.S.). The radiographs were accepted or rejected for evaluation based on the clarity of the
implant threads. All readable radiographs
were uploaded to an image analysis software
package (DfW 2.8, SOREDEX) that was calibrated using the known length or diameter of
the dental implants and displayed on a 24 in.
LCD screen (iMac, Apple, Calif., U.S.) and evaluated under standardized conditions (ISO
12646:2004). The marginal bone levels were
determined from linear measurements performed by an independent calibrated examiner
on each periapical radiograph, from the mesial
and distal margin of the implant neck to the
most coronal point where the bone appeared
to be in contact with the implant.
– Insertion torque. This was recorded at implant
placement by the same surgeon (MT) using
the iChiropro surgical unit (Bien-Air, Bienne,
Switzerland).
– Implant stability quotient (ISQ): The measurements were performed at implant placement
and at the six-month follow-up by the surgeon
(MT) using resonance frequency analysis
(Osstell Mentor device, Osstell, Gothenburg,
Sweden).
– Residual alveolar bone quality: This was
assessed during surgery by the same surgeon
(MT) and classiﬁed according to the Lekholm
and Zarb classiﬁcation.

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Table 1
Drilling protocols.

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Physiological bone remodeling on Osstem implants

Fig. 1

Fig. 2

Fig. 3

Fig. 1
Preoperative panoramic
radiograph.
Fig. 2
Preoperative intraoral
photograph: lateral view.
Fig. 3
Preoperative intraoral
photograph: occlusal view.

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Physiological bone remodeling on Osstem implants

Fig. 4

Fig. 5

conﬁdence interval (CI), whereas ordinal and
dichotomous variables are presented as percentages. The implant or the restoration were
the statistical units of analysis. Differences in
the proportion of patients with prosthesis failures, implant failures and complications (dichotomous outcomes) were compared between the
groups using the Fisher exact test. Differences
in mean for continuous outcomes (bone level
and ISQ) were compared at patient level by independent samples t-tests and one-way analysis of variance, respectively. Comparisons
between each time point and the baseline measurements were made by paired tests, in order
– Thickness of the gingival biotype: This was to detect any changes in marginal periimplant
assessed at the time of surgery using a perio- bone levels. All statistical comparisons were
dontal probe (PCPUNC156, Hu-Friedy Italy, conducted at the 0.05 level of signiﬁcance.
Milan, Italy) or a tension-free caliper. The gingival biotype was considered thin if the meaResults
surement was 1 mm and thick if > 1 mm.
Statistical analysis

Patients data were collected in an MS Excel
spreadsheet. A statistician with expertise in
dentistry analyzed the data and performed all
of the statistical analysis using SPSS for Macintosh (Version 22.0; IBM, Chicago, Ill., U.S.). The
distributions of continuous variables are given
as mean ± standard deviation, median and 95%

A total of 243 sandblasted and acid-etched bone
level implants featuring an 11° Morse taper connection were placed in 90 consecutive patients
recruited and treated between September 2014
and December 2015 and followed for at least one
year after loading. All of the initially selected patients were included and no patients dropped out
of the study. The data of all of the patients were
evaluated in the statistical analysis.

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Fig. 4
Virtual planning. From left to
right, teeth #47, 46 and 44.
Fig. 5
Periapical radiograph taken
after placement of the
implants.

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Physiological bone remodeling on Osstem implants

Figs. 6 & 7

Figs. 8 & 9

Fig. 6
Screw-retained temporary
restoration placed eight weeks
after implant placement.
Fig. 7
Try-in of the zirconia-based
frameworks.
Fig. 8
Delivery of the ﬁnal
restoration.
Fig. 9
Intraoral photograph taken
one year after delivery of the
deﬁnitive restoration.

The patients were of both sexes (34 males and
56 females) and had an average age of
53.2 ± 15.4 years (range of 24–81 years). All of
the patients were followed up for a minimum
period of one year after loading (mean of
17.6 ± 2.5 months; range of 12–24 months). Most
of the implants (n = 208) were placed in nonsmoking patients, while 20 implants were
placed in patients who smoked ≤ 10 cigarettes
per day and 15 implants in patients who smoked
> 10 cigarettes per day. The main implant characteristics are shown in Table 2.
Forty-three implants were immediately
placed in post-extraction sockets (Type 1),18 75
implants were placed 12–16 weeks after a socket preservation procedure (Type 3)18 and 125
implants were placed late (more than four
months after tooth extraction, Type 4).18 Forty-nine implants were immediately loaded
(20.2%) and 76 implants were placed using guided surgery (32.5%). Overall, 172 implants were
conventionally placed without bone augmentation. Nineteen implants were placed in conjunction with horizontal GBR using a native collagen
membrane and 1:1 ratio of particulated xenograft
and autologous bone. Ten implants were placed
in conjunction with a transcrestal sinus ﬂoor
elevation. Three implants were placed with a
combination of GBR and transcrestal sinus ﬂoor
74 Volume 3 | Issue 1/2017

elevation. Thirty-nine immediate implants were
placed in combination with socket preservation
procedures.
The overall insertion torque ranged between
15.0 and 45.0 N cm (mean of 42.9 ± 4.8 N cm).
Two hundred and three implants (83.5%) were
placed at an insertion torque ranging from ≥ 35
to 45 N cm. The deﬁnitive restorations were
delivered 8 to 20 weeks after second-stage surgery (Fig. 11). All of the impressions were taken
at implant or abutment level with anatomically
customized light-curing acrylic impression trays
(Elite LC tray, Zhermack, Badia Polesine, Italy)
fabricated on a preliminary cast derived from an
irreversible hydrocolloid impression taken with
a stock metal impression tray. The impressions
were made with plaster (Snow White Plaster
No. 2, Kerr, Orange, Calif., U.S.) in the case of
edentulous patients or with a polyether material
(Impregum Penta, 3M Italia, Milan, Italy) for
single and partial restorations.
Overall, 104 single crowns were delivered in
67 patients, 20 ﬁxed partial dentures (FPDs)
supported by two to three implants were delivered in 16 patients and the remaining 16 patients
received 19 full-arch restorations supported by
two to six implants (Table 3). Deﬁnitive prostheses were screwed on to 168 implants (71
single crowns, 11 FPDs and 13 full-arch resto-

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Fig. 10

rations) and cemented on to the remaining
61 implants (33 single crowns, nine FPDs and
one full-arch restoration). Three patients (six
implants) received overdentures on OT Equator
attachments (Rhein 83, Bologna, Italy) and two
patients (eight implants) received overdentures
fully supported by a titanium CAD/CAM bar
(New Ancorvis) and OT Equator attachment
screwed on the top.
Five implants failed in ﬁve patients, resulting
in a cumulative implant survival rate of 97.9% at
the follow-up one year after loading. All of those
implants failed before deﬁnitive loading. Two
implants were placed in combination with bone
augmentation procedures (p = 0.6310), one implant was immediately loaded (p = 1.000) and
two were placed immediately after tooth extraction (p = 0.2108). Of these, two implants were
placed using guided surgery (p = 0.6572). No
statistically signiﬁcant differences were found
(p > 0.05). Two out of seven implants placed at an
insertion torque of < 35 N cm failed (p = 0.0068).
No deﬁnitive prosthesis failed, resulting in a
cumulative prosthetic survival rate of 100%.
Four patients experienced one technical complication each, resulting in a cumulative prosthetic
success rate of 97.2% at the follow-up one year
after loading. One zirconia-based, full-arch
framework, delivered on six implants, presented
a misﬁt between the framework and the most
distal implant at the try-in appointment. The
framework was remade with no further complications. One zirconia-based, full-arch, screwretained restoration, delivered on six implants,
fractured at the bisque bake try-in appointment.
The restoration was remade with no further
complications. Two patients with a single
screw-retained restoration experienced screw
loosening. The screws were replaced chairside
with no further complications. One patient ex-

perienced pain and swelling up to 3 weeks after
implant placement, resulting in a MBL greater
than 2 mm. Nevertheless, no further pathological MBL was experienced.
Most of the implants were placed at crest
level or a little below. In the case of post-extractive
implants, they were placed 1.0–1.5 mm below the
buccal bone plate. At the deﬁnitive prosthesis
delivery, the mean MBL was 0.26 ± 0.25 mm
(95% CI: 0.27–0.30). The cumulative mean MBL
between implant placement and the one year
after loading follow-up was 0.37 ± 0.25 mm (95%
CI: 0.26–0.30). The MBL in the interval between
the deﬁnitive prosthesis delivery and the one year
after loading follow-up was 0.11 ± 0.14 mm (95%
CI: 0.08–0.10). Overall, 86.8% of the implants
(n = 211) showed an MBL of ≤ 0.5 mm one year
after loading, while only three implants showed
an MBL of > 1.0 mm. Two patients were asymptomatic, while a third patient presented with pain
without suppuration. This patient was treated
with an antibiotic and analgesic until the resolution of the pathology. Eighty-two out of 243 patients (33.7%) reached the two-year follow-up.
In this cohort of patients, MBL between the oneand the two-year follow-up was 0.05 ± 0.14 mm
(range of 0.0–0.2 mm; 95% CI: -0.01–0.10).
Comparison of MBL and the investigated risk
factors found statistically higher MBL for smokers, a thin gingival biotype and GBR. Immediate
loading and placement of the deﬁnitive abutment
on the day of surgery were found to be protective
factors, with statistically signiﬁcantly lower MBL.
Most of the implants (n = 203; 83.5%)
reached an insertion torque of 45 N cm. The
other 40 implants were placed at an insertion
torque ranging from ≥ 35 to < 45 N cm (n = 33;
13.6%), > 25 to < 35 N cm (n = 4; 1.6%) and
< 25 N cm (n = 3; 1.3%). No statistically signiﬁcant correlation was found between insertion
torque and MBL (p = 0.3726).
At implant placement, the mean ISQ value
was 71.6 ± 5.5 (range of 45–88); At the sixmonth follow-up, mean ISQ was 76.7 ± 4.4
(range of 66–89). The difference was statistically signiﬁcant (p = 0.0001).
One hundred and sixty-six implants were
placed in bone of Type 1 and 2 quality (n = 18).
The remaining 77 implants were placed in Type
3 and 4 bone. No statistically signiﬁcant correlation was found between insertion torque and
MBL (p = 0.4216).
A thin gingival biotype was associated with
higher MBL compared with a thick biotype.
The difference was statistically significant

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Fig. 10
Periapical radiograph taken
one year after delivery of
the deﬁnitive restoration.

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Table 2
Implant characteristics.

Table 2

Table 3
Type of restoration.
Fig. 11
Timing of implant placement
and loading according to the
surgical and prosthetic
protocol adopted.
Table 4
Marginal bone loss associated
with different risk factors.

7.0 mm

8.5 mm

10.0 mm

11.5 mm

13.0 mm

TOTAL

Osstem TSIII
3.0 mm

–

–

–

–

4

4

Osstem TSIII
3.5 mm

–

2

6

27

10

45

Osstem TSIII
4.0 mm

3

2

17

31

14

67

Osstem TSIII
4.5 mm

3

8

18

8

20

57

Osstem TSIII
5.0 mm

–

1

20

9

–

30

Osstem TSIII
6.0 mm

–

2

11

3

–

16

Osstem TSIII
7.0 mm

–

4

15

5

–

24

TOTAL

6

19

87

83

48

243

Central
incisors

Lateral
incisors

Canines

Premolars

Molars

TOTAL

Maxilla

26

7

4

45

41

123

Mandible

–

15

5

42

58

120

TOTAL

26

22

9

87

99

243
Fig. 11

Table 3

Single
restoration

Fixed partial
denture

Overdenture
on OT Equator

Overdenture
on titanium bar

Fixed full-arch
restoration

TOTAL

Maxilla

46

9

1

–

7

63

Mandible

58

11

2

2

7

80

TOTAL

104

20

3

2

14

143

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Table 4

p-value
Implant location

Timing of implant placement

Type of implant placement

Type of prosthesis retention

Type of implant loading

Bone augmentation

Insertion torque

Bone density

Smoking

Immediate abutment

Gingival biotype

Maxilla (n = 123)

Mandible (n = 120)

0.36 ± 0.29

0.38 ± 0.23

Post-extractive (n = 43)

Delayed (n = 75)

Healed site (n = 125)

0.36 ± 0.29

0.37 ± 0.27

0.38 ± 0.30

Guided

Conventional freehand

0.36 ± 0.24

0.37 ± 0.26

Cemented (n = 78)

Screwed (n = 165)

0.38 ± 0.20

0.36 ± 0.23

Immediate

Early/conventional

0.26 ± 0.20

0.40 ± 0.26

0 (n = 172)

1 (n = 19)

2 (n = 10)

0.7961

0.8544

0.5135

0.0003

3 (n = 3)

4 (n = 39)

0.35 ± 0.19 0.51 ± 0.50 0.22 ± 0.19 0.23 ± 0.06

0.39 ± 0.27

≤ 35 N cm (n = 40)

≥ 35–45 N cm (n = 203)

0.42 ± 0.44

0.36 ± 0.21

Types 1 and 2 (n = 166)

Types 3 and 4 (n = 77)

0.36 ± 0.23

0.39 ± 0.31

Nonsmoker (n = 222)

Smoker, ≥ 10 cigarettes per day (n = 21)

0.35 ± 0.22

0.48 ± 0.38

Yes (n = 26)

No (n = 217)

0.25 ± 0.19

0.38 ± 0.26

Thin (n = 78)

Thick (n = 165)

0.43 ± 0.27

0.34 ± 0.25

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0.0000

0.3726

0.4216

0.0098

0.0113

0.0307

[78] => JOSR_A4_Editorial_03.qxp_Layout 1

Physiological bone remodeling on Osstem implants

(p = 0.0307). All of the radiographic compari- Immediate loading and the placement of a deﬁnsons are reported in Table 4.
itive abutment at implant insertion and never
removed have been proven to reduce MBL.22, 23 A
possible explanation of this phenomenon could
Discussion
be that most of the immediately loaded implants
were placed without a ﬂap, using guided surgery,
The aim of this prospective open-cohort study and received the deﬁnitive abutment on the day
was to investigate, over a 1 year after loading of surgery, minimizing MBL.
period, the implant survival and success rates of
High primary implant stability is considered
sandblasted and acid-etched bone level implants one of the main factors necessary for achieving
featuring an 11° Morse taper connection placed a predictable high success rate.24–28 Nevertheless,
in private practice, and to evaluate the physiolog- there is no consensus as to the ideal insertion
ical marginal bone remodeling among subgroups torque required to prevent implant failure. In the
of exposed and unexposed subjects. The main present study, two out of seven implants placed
limitation of the present study was the short fol- at an insertion torque of < 35 N cm failed, reachlow-up period. Nevertheless, one year after load- ing a statistically signiﬁcant difference. In the
ing is sufficient to evaluate the physiological study, 83.5% of the implants were placed at an
marginal bone remodeling that was the main insertion torque of 45 N cm. The drilling protocol
topic of this research.
was customized according to the bone density.
In the present study, ﬁve out of 243 implants Conventional preparation was performed in
failed over a period of one year after loading, healed sites with a bone density of Type 2 or 3.20
resulting in a cumulative implant survival rate of Narrow or halfway adapted preparations were
97.9%. No deﬁnitive prosthesis failed. One bio- performed in the case of post-extractive implants
logical and four technical complications were and poor bone quality, using freehand or guided
experienced, resulting in a cumulative prosthetic surgery, respectively. Finally, the osteotome techand implant success rate of 97.2 and 99.6%, nique was performed only in the maxilla, in order
to perform bone spreading.
respectively.
The major clinical conclusion of the present
research was that the physiological marginal
Conclusion
bone remodeling using Osstem TSIII implants
(Osstem) was 0.37 mm within one year after
loading, independent of the surgical and pros- Low implant failure and physiological marginal
thetic protocols. Subgroup analysis showed that bone remodeling of 0.37 mm within one year
smoking, a thin tissue biotype and GBR were after loading can be expected using Osstem TSIII
associated with a statistically significantly implants in the daily practice. Smoking, GBR and
higher MBL. This supports Sgolastra et al.’s con- a thin tissue biotype were associated with higher
clusion that smoking seems to be positively as- MBL, while immediate loading and placement
sociated with higher MBL, implant failure and of the deﬁnitive abutment on the day of surgery
risk of periimplantitis.19
reduced the MBL.
The results of the present study are in agreement with a recent systematic review and metaanalysis that showed that implants placed with
Competing interests
an initially thicker periimplant soft tissue have
less radiographic MBL in the short-term follow- The first author (MT) is the Research Project
up.20 The results of this study also demonstrat- Manager at Osstem AIC, Italy. However, this
ed that implants placed with GBR are as suc- research was self-supported. Hence, the
cessful as implants placed into sites with pristine authors declare that they have no competing
bone. In the present study, the mean MBL expe- interests.
rienced around the implants placed in regenerated bone was slightly higher than that of the
implants placed in nongrafted sites. No strong
Acknowledgments
evidence is associated with higher MBL and GBR
procedures. Nevertheless, data reported in the Dr. Marco Tallarico wishes to thank Ms. Gianina
present study are consistent with, or slightly Bizduna and Stephany Zambrano for their imlower than, that reported in previous studies.21 portant clinical assistance.
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Physiological bone remodeling on Osstem implants

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Volume 3 | Issue 1/2017 79

[80] => JOSR_A4_Editorial_03.qxp_Layout 1

Guidelines for authors

Authors must adhere
to the following guidelines
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It is preferred that there be no more than six authors.
If more authors have participated in the study, the
Patients have a right to privacy that should not be violated without informed consent. contribution of each author must be disclosed at the
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Title
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The manuscript must contain an abstract and a minimum of 3, maximum of 6 keywords. The abstract
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stract and list of captions, but including the references, may be a maximum of 4,000 words. ExcepCompeting interests
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General

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Guidelines for authors

gether, then use lowercase letters to designate these
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[cover] =>

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Table of contents

[toc_titles] =>

[cached] => true )