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viernes, 30 de agosto de 2013

A NEW IMPLANT DESIGN FOR CRESTAL BONE PRESERVATION: INITIAL OBSERVATIONS AND CASE REPORT




Harold Baumgarten, DMD* • Roberto Cocchetto, DDS, MD† • Tiziano Testori, DDS, MD‡
Alan Meltzer, DMD, MScD§ • Stephan Porter, DDS, MSD, MS||
Pract Proced Aesthet Dent 2005;17(10):735-740 735
Following the exposure and restoration of two-piece dental implants, some change
in the vertical level of the peri-implant crestal bone height has been reported. This
change in crestal bone height has not, however, negatively impacted long-term
implant success. This article describes how the concept of platform switching is
incorporated into a new implant design as a means of reducing or eliminating the
occurrence of crestal bone loss. Preliminary observations from clinicians utilizing
this new implant design are herein presented.
Learning Objectives:
This article discusses an inflammatory mechanism involved in crestal bone loss
following implant restoration. Upon reading this article, the reader should:
• Be able to identify a mechanism involved in crestal bone loss following
implant exposure.
• Understand how the concept of platform switching as a means of reducing
or eliminating this occurrence is incorporated into a new implant design.
Key Words: implant, bone, resorption, platform switching
N O V E M B E R / D E C E M B E R B A U M G A R T E N
17
10
* Clinical Professor, Department of Periodontics, University of Pennsylvania, School of Dental
Medicine, Philadelphia, PA; private practice, Philadelphia, PA.
†Private practice, Verona, Italy.
‡Assistant Clinical Professor and Head of the Section of Implant Dentistry and Oral
Rehabilitation, Department of Odontology, Galeazzi Institute, Milan, Italy; private practice,
Como, Italy.
§Diplomate, American Academy of Periodontology; Associate Clinical Professor, Department
of Implant Dentistry, New York University College of Dentistry, New York, NY; private practice,
Voorhees, NJ.
||Private practice, West Palm Beach, FL, and Windsor, United Kingdom.
Harold Baumgarten, DMD,100 S. Broad Street, Philadelphia, PA 19110
Tel: 215-568-8130 • E-mail: hbaumgarten@4dentistry.com
Postrestorative reductions in crestal bone height around
endosseous dental implants have long been acknowledged
to be a normal consequence of implant therapy
involving two-stage hexed implants.1-4 Such remodeling
does not typically occur as long as the implant remains
completely submerged, but rather develops when an
abutment is connected during second-stage surgery,
when a two-stage implant is placed and connected to
an abutment in a one-stage procedure, or when an
implant is prematurely exposed to the oral environment
and bacteria.5
Research by Hermann, et al demonstrated that crestal
bone loss typically occurs approximately 2 mm apical
to the implant-abutment junction (IAJ).6 This position
appears to be constant, regardless of where the IAJ is
situated relative to the original level of the bony crest.6
The researchers also demonstrated that the addition of
a textured, bone-holding surface within 0.5 mm of the
IAJ fails to prevent bone resorption within 2 mm apical
to the IAJ.6
Investigations by various researchers offered explanations
on why the presence of the IAJ appears to trigger
resorption in the adjacent bone. Ericsson, et al found
histologic evidence of inflammatory cell infiltrate associated
with a 1-mm– to 1.5-mm–tall zone adjacent to
the IAJ.7 Berglundh and Lindhe concluded that approximately
3 mm of peri-implant mucosa is required to create
a mucosal barrier around a dental implant.8 This
suggests that crestal bone remodeling may occur to
create space when inadequate soft tissue height is present
so that a biological seal can be established, which
will isolate the crestal bone and protect it from the
oral environment.
These investigations have focused on implant
systems in which the diameter of the implant-seating
surface matches that of the abutment. This ubiquitous
design positions the abutment inflammatory cell infiltrate
in direct approximation to the crestal bone at the
time of abutment connection.
Platform Switching
The concept of “platform switching” refers to the use
of a smaller-diameter abutment on a larger-diameter
implant collar; this connection shifts the perimeter of
the IAJ inward toward the central axis (ie, the middle)
of the implant.5 Lazzara and Porter theorize that
the inward movement of the IAJ in this manner also
shifts the inflammatory cell infiltrate inward and away
from the adjacent crestal bone, which limits the bone
change that occurs around the coronal aspect.5
Crestal bone preservation has been reported on other
commercially available implant designs, purportedly
736 Vol. 17, No. 10
Practical Procedures & AESTHETIC DENTISTRY
Figure 4. Occlusal view of the sockets taken
after extraction. To avoid the risk of altering the
soft tissue profile, a flap was not reflected.
Figure 1. Diagram of the Certain Prevail implant.
Note implant body and implant collar taper to
the restorative platform for standard prosthetics.
Figure 2. Preoperative facial view of nonrestorable
fractured and carious central incisors.
Figure 3. Initial radiograph where the central
incisors had been endodontically treated and the
margins were fractured apical to the crestal bone.
attributed to microthreads at the coronal aspect of
the implant, connection designs, occlusal schemes, or
combinations thereof.9
In 1991, Implant Innovations, Inc. (3i, Palm Beach
Gardens, FL) introduced 5-mm– and 6-mm–diameter
implants with seating surfaces (ie, restorative platforms)
of the same dimensions. These large-diameter implants,
with a larger surface area, were intended to increase the
amount of bone-to-implant contact when placing shorter
implants in areas of limited bone height, such as under
the maxillary sinus or above the inferior alveolar canal.
The ability to increase the bone-to-implant contact by the
use of wide-diameter implants also enhanced the likelihood
of achieving primary stability in areas of poor-quality
bone. At the time of the wide-diameter implants’
introduction, no matching, similarly dimensioned prosthetic
components were available. Hence, clinicians
restored them with standard 4.1-mm abutments.
After a 5-year period, the typical pattern of crestal
bone resorption was not observed radiographically in
cases where platform switching was utilized. Lazzara
and Porter theorize that this occurred because shifting
the IAJ inward also repositioned the inflammatory cell
infiltrate and confined it within a 90° area that was not
directly adjacent to the crestal bone.
The ability to reduce or eliminate crestal bone loss
can result in significant aesthetic and clinical benefits.
In order to facilitate the practice of platform switching,
the Certain Prevail Implant (3i, Implant Innovations, Inc.,
Palm Beach Gardens, FL) has been developed. Its design
utilizes the Osseotite dual acid-etched surface, which
maximizes the contact of bone to implant. The performance
of the original Osseotite implant (an externalhexed,
parallel-walled, hybrid design) has been shown
in both in vitro and in vivo studies to perform differently
from machine-surfaced versions.10-14
The coronal aspect of the Certain Prevail Implant
is designed to be slightly wider than the diameter of the
straight-walled implant body, flaring out at approximately
a 30° angle and resulting in a collar diameter of 4.8 mm
(Figure 1). This expanded collar can provide better
engagement of the bone crest, better sealing of extraction
sockets, and better primary stability. The collar then
bevels back at a 15° angle to provide a color-coded
restorative platform with a diameter of 4.1 mm. Restoring
the 4.8-mm implant collar with the corresponding 4.1-
mm prosthetic component shifts the IAJ inward, moving
the inflammatory infiltrate away from the surrounding
bone. To achieve this effect and maintain adequate softtissue
depth, the implant should be placed crestally if
sufficient soft tissue height and/or interocclusal space
is present, or subcrestally if insufficient soft tissue height
and/or interocclusal space is present.
P P A D 737
Baumgarten
Figure 8. Occlusal view of implants with healing
abutments in place postoperation. The interdental
papillae were not disturbed during the surgery.
Figure 5. Clinical occlusal view of the surgical
guide in place. The planned implant placement
was identified by the holes in the surgical guide.
Figure 7. Periapical radiograph taken immediately
after implant placement. Note the vertical
height of the interimplant bone.
Figure 6. Clinical occlusal view of the implants in
place. Note that the interdental papillae were
maintained throughout the procedure.
Case Presentation
A 28-year-old male presented with nonrestorable maxillary
central incisors that had previously been treated
endodontically, and then were subsequently fractured by
trauma (Figures 2 and 3). The teeth were carefully
extracted and, with the aid of a surgical guide, two 5.0-
mm x 13-mm implants (ie, Certain Prevail, 3i, Palm Beach
Gardens, FL) were placed in a single-stage protocol
(Figures 4 through 8). The specific implant diameters and
lengths were selected by the clinician based on the size
and shape of the individual sockets. The implants were
placed in a flapless manner in order to protect the buccal
cortical plate from injury to the vascular supply, which
is often associated with a full-thickness flap. Moreover,
great care was taken to avoid touching the buccal plate
of the sockets during implant site preparation.
Healing abutments with 5-mm emergence profiles
and 4.1-mm restorative platforms were immediately placed
(Figures 9 and 10). The patient was then discharged with
antibiotic and anti-inflammatory prescriptions.
After 3 days, two 4.1-mm customizable abutments
(ie, GingiHue Posts, 3i, Palm Beach Gardens, FL), prepared
by the dental technician on the master cast were
inserted into the internal interface of the implants and
torqued to 20 Ncm (Figures 11 through 14). These titanium
abutments have a gold-nitride coating that eliminates
graying of the marginal gingival tissue. Two acrylic
provisional crowns were then luted to the abutments with
temporary cement and adjusted out-of-occlusal contact,
following the protocol of immediate nonocclusal loading
(Figure 15).15 An intraoral radiograph was taken (Figure
16), and the patient was instructed to avoid loading
the crowns for any purpose for at least eight weeks.
Gentle brushing with a toothpaste containing chlorhexidine,
was recommended.
Following a 2-month healing period (Figure 17),
clinical osseointegration was confirmed and two metalceramic
crowns were placed. The prognosis for maintenance
of the interdental papillae was excellent.
The definitive crowns were constructed on duplicate
abutments made from a surgical index at the time of
implant placement.
No additional implant-level impression procedure
was required due to the technical prosthetic protocol,
which allowed the construction of the definitive crowns
Figure 9. Radiograph of the two implants with the
4-mm–diameter healing abutments in place. Note that the
implant restorative platforms were subcrestal.
Figure 12. Two provisional crowns splinted together on the
prepared implant abutments.
Figure 10. Occlusal view of master cast with soft tissue
replicated in resilient material. The implant restorative platforms
are color coded to simplify the restorative process.
Figure 11. View of the prepared abutments on the model.
Platform switching is a design feature of the Certain
Prevail Implant.
738 Vol. 17, No. 10
Practical Procedures & AESTHETIC DENTISTRY
on a duplicated model and their subsequent delivery
chairside (Figures 18 and 19).
Discussion
Clinical observation of the bone-preserving effects of
platform switching has been ongoing for more than a
decade. This procedure has been used by a number of
clinicians successfully around the world.
The procedure requires that the “switch” be in place
from the day the implant is uncovered or exposed to the
oral cavity in either a one- or two-stage approach. It cannot
be utilized after the establishment of the biologic
width around a conventional implant-abutment interface
configuration to regain crestal bone height. Potential
applications include situations where a larger implant is
desirable, but the prosthetic space is limited, in the aesthetic
zone; where preservation of the crestal bone can
lead to improved aesthetics; and where shorter implants
must be utilized.
It is important to note that sufficient tissue depth
(approximately 3 mm or more) must be present to accommodate
an adequate biologic width. In the absence of
sufficient soft tissue, bone resorption will likely result,
regardless of the implant geometry.16-19 This sometimes
requires that the implant platform be placed below the
bone crest to obtain adequate tissue depth. Additionally,
sufficient ridge width (ie, a minimum of 6.8 mm) must be
present to accommodate the flared 4.8-mm implant collar.
Case selection and management, however, may influence
the clinical outcome and radiographic evidence of
crestal bone preservation.
While bone preservation has been observed for
some time as a result of the use of a standard-diameter
abutment on a wider-diameter implant, the potential for
confusion has existed for clinicians who have attempted
to employ this strategy while using standard components.
Laboratories and restorative dentists are accustomed to
working with matching-diameter implants and abutments.
The color-coordinated scheme of the Certain Prevail
Implant has been designed to ensure that the diameter
of the implant-seating surface and the restorative platform
of the abutment match, minimizing the possibility
of confusion at the time of component selection, dentallaboratory
processing, and prosthetic selection.
Figure 13. View of the peri-implant soft tissues and
implant restorative platforms three days after placement.
Note advanced healing of the soft tissues.
Figure 14. Facial view of the prepared abutments in place.
Their gold-colored titanium nitride coating helps to mask
the metallic color of the titanium abutments.
Figure 15. Facial view of the provisional crowns immediately
after cementation. The peri-implant soft tissues will
adapt to the provisional crown contours.
Figure 16. Radiograph at abutment connection, three days
after implant placement. The implant restorative platforms
of the abutments and implants are subcrestal.
P P A D 739
Baumgarten
Conclusion
Preliminary evidence suggests that the anticipated bone
loss that occurs around two-stage hexed implants
may be reduced or eliminated when implants are
restored with smaller-diameter abutments, a practice
termed platform-switching.5 A new implant design
has been developed that facilitates this practice,
and initial clinical observations indicate the preservation
of crestal bone results. Definitive clinical trials are
currently underway.
References
1. Albrektsson T, Zarb G, Worthington P, Eriksson AR. The longterm
efficacy of currently used dental implants: A review and
proposed criteria of success. Int J Oral Maxillofac Impl
1986;1(1):11-25.
2. Smith DE, Zarb GA. Criteria for success of osseointegrated
endosseous implants. J Prosthet Dent 1989;62(5):567-572.
3. Bengazi F, Wennestrom JL, Lekholm U. Recession of the soft tissue
margin at oral implants: A 2-year longitudinal prospective
study. Clin Oral Implants Res 1996;7(4):303-310.
4. Morris HF, Ochi S. The influence of implant design, application,
and site on clinical performance and crestal bone: A multicenter,
multidisciplinary clinical study. Dental Implant Clinical
Research Group (Planning Committee). Implant Dent 1992;1(1):
49-55.
5. Lazzara RJ, Porter SS. Platform switching: A new concept in
implant dentistry for controlling post-restorative bone levels.
Accepted for Publication, 2006 Int J Perio Rest Dent.
6. Hermann JS, Schoolfield JD, Nummikoski PV, et al. Crestal bone
changes around titanium implants: A methodologic study comparing
linear radiographic with histometric measurements. Int J
Oral Maxollofac Impl 2001;16(4):475-485.
7. Ericsson I, Persson LG, Berglundh T, et al. Different types of inflammatory
reactions in peri-implant soft tissues. J Clin Periodontol
1995;22(3):255-261.
8. Berglundh T, Lindhe J. Dimension of the periimplant mucosa.
Biologic width revisited. J Clin Periodontol 1996;23(10):
971-973.
9. Morris HF, Winkler S, Ochi S, Kanaan A. A new implant
designed to maximize contact with trabecular bone: Survival to
18 months. J Oral Implantol 2001;27(4):164-173.
10. Lazzara RJ, Testori T, Trisi P, et al. A human histologic analysis
of Osseotite and machined surfaces using implants with two
opposing surfaces. Int J Periodont Rest Dent 1999;19:117-129.
11. Khang W, Feldman S, Hawley CE, Gunsolley J. A multicenter
study comparing DAE and machined-surfaced implants in various
bone qualities. J Periodontol 2001;72(10):1384-1390.
12. Bain CA, Weng D, Meltzer A, et al. A meta-analysis evaluating
the risk for implant failure in patients who smoke. Compend
Cont Educ Dent 2002;23(8):695-699, 702, 704.
13. Stach RM, Kohles SS. A meta-analysis examining the clinical survivability
of machined-surfaced and Osseotite implants in poorquality
bone. Implant Dent 2003;12(1):87-96.
14. Feldman S, Boitel N, Weng D, et al. Five-year survival distributions
of short-length (10 mm or less) machined-surfaced and
Osseotite implants. Clin Implant Dent Relat Res 2004;6(1):
16-23.
15. Cocchetto R, Vincenzi G. Delayed and immediate loading of
implants in the aesthetic zone: A review of treatment options.
Pract Proced Aesthet Dent 2003;15(9):691-698.
16. Todescan FF, Pustiglioni FE, Imbronito AV, et al. Influence of the
microgap in the peri-implant hard and soft tissues: A histomorphometric
study in dogs. Int J Oral Maxillofac Impl 2002:17(4):
467-472.
17. Hermann JS, Cochran DL, Nummikoski PV, Buser D. Crestal bone
changes around titanium implants. A radiographic evaluation of
unloaded nonsubmerged and submerged implants in the canine
mandible. J Periodontol 1997;68(11):1117-1130.
18. Herman J, Buser D, Schenk R, et al. Biologic width around oneand
two-piece titanium implants. A histomorphometric evaluation
of unloaded nonsubmerged and submerged implants in the
canine mandible. Clin Oral Impl Res 2001;12:559-571.
19. Gaucher H, Bentley K, Roy S, et al. A multi-centre study of
Osseotite implants supporting mandibular restorations: A 3-year
report. J Can Dent Assoc 2001;67(9):528-533.
Figure 17. Clinical view of the soft tissue healing eight
weeks after implant placement. The underlying bone supports
the interdental papillae.
Figure 19. Postoperative facial view of the definitive
restoration in place. The final crowns were splinted for
greater stability at the request of the patient, who had had
the provisionals splinted.
740 Vol. 17, No. 10
Practical Procedures & AESTHETIC DENTISTRY
Figure 18. Radiograph of the definitive restoration. Note
minimal remodeling of the interproximal bone and the
absence of bone loss relative to restorative platforms.

Journal of Biomaterials Applications

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Journal of Biomaterials Applications
http://jba.sagepub.com/content/early/2011/01/28/0885328210396946
The online version of this article can be found at:
DOI: 10.1177/0885328210396946
J Biomater Appl published online 22 February 2011
Ferreira Junior
Etiene Andrade Munhoz, Augusto Bodanezi, Tania Mary Cestari, Rumio Taga, Paulo Sergio Perri de Carvalho and Osny
Long-term rabbits bone response to titanium implants in the presence of inorganic bovine-derived graft
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Article
Long-term rabbits bone response
to titanium implants in the presence
of inorganic bovine-derived graft
Etiene Andrade Munhoz1, Augusto Bodanezi2,
Tania Mary Cestari3, Rumio Taga3, Paulo Sergio Perri de
Carvalho1 and Osny Ferreira Junior1
Abstract
This study evaluated bone responses to titanium implants in the presence of an inorganic graft material. The bilateral
mandible incisors of 24 rabbits were surgically extracted and one of the exposed sockets, chosen at random, was filled
with an inorganic xenogenic bone graft (Gen-ox ), whereas the remaining socket was left to heal naturally and served as
a control. After 60 days, titanium implants were inserted in the specific areas, and on days 0, 30, 60, and 180 after the
implant insertions, six animals of each group were killed. Digital periapical radiography of implant region was obtained
and vertical bone height (VBH) and bone density (BD) were evaluated by digital analysis system. In the undecalcified
tissue cuts, bone-to-implant contact (BIC) and bone area (BA) within the limits of the implant threads were evaluated and
compared statistically by means of two-way ANOVA and Tukey’s test ( <0.05). No significant differences were detected
in VBH and BA, either between groups or between different experimental intervals. The BD was significantly higher in
the experimental group than in the control group in all the intervals tested, but there were no significant differences by
interval. The BIC was statistically lower in the control group on day 0; however, a significant increase was observed on
days 60 and 180 ( <0.05). The use of an inorganic xenograft prior to insertion of a titanium implant did not interfere
with the course of osseointegration.
Keywords
inorganic xenograft, titanium implants, osseointegration
Introduction
The maintenance of height, thickness, and quality of
bone in order to provide an adequate implant placement
and prosthetic rehabilitation1 is a constant challenge
after surgical procedures that involve hard tissue
removal. To address this problem, filling of the bone
defect with a graft has been recommended.2–6
Autologous bone is undoubtedly the best graft material
for this purpose due to the biocompatibility;3 however,
its scarcity and significant post-procedural
morbidity makes its use limited and difficult. For
these reasons, it is important to find alternative graft
substitutes that present satisfactory characteristics of
biocompatibility, osseointegration, and availability as
well as inductive and conductive properties.
In this context, the inorganic version of bovine
xenografts has demonstrated remarkable
osteoconductive properties.4,5 These include the
hydroxyapatite mineral content, a porous architecture
that allows for a trabecular network to be formed,
biomechanical properties similar to that of human
cancellous bone5 and the absence of immunological
and inflammatory responses that are elicited.4
Journal of Biomaterials Applications
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! The Author(s) 2011
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DOI: 10.1177/0885328210396946
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1Department of Stomatology and Oral Surgery, School of Dentistry,
University of Sa˜o Paulo, Bauru, Brazil.
2Department of Conservative Dentistry, School of Dentistry, Federal
University of Rio Grande do Sul, Porto Alegre, Brazil.
3Department of Oral Biology, School of Dentistry, University of Sa˜o
Paulo, Bauru, Brazil.
Corresponding author:
Etiene Andrade Munhoz, Department of Stomatology and Oral Surgery,
School of Dentistry, University of Sa˜o Paulo, Al. Dr. Ota´vio Pinheiro
Brisolla 9-75, 17012-901, Bauru, Sa˜o Paulo, Brazil
Email: etiamfob@yahoo.com
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When a titanium implant is inserted in a grafted
area, a bone-like response, in the form of high quality
osseointegration, is expected to occur.7 It is known that
xenograft materials can establish desirable connective
tissues and cancellous bone interactions during the first
stages after implant insertion; however, this configuration
may be unfavorable at later periods when implant
stability must be acquired.8,9
The microscopic responses of medullary bone to
biomaterials and titanium implants had been reported
separately and in a few short-term investigations.
3–6,10–16 In an opposite way, Ferreira et al.10
showed recently new bone formation on sinus lift
augmentation on humans 3 years after grafting and
socket’s implant insertion.
To achieve specific evidences on responses of
combined procedures, this prospective study aimed to
evaluate the influence of an inorganic xenograft filled
on rabbit’s mandible sockets on the maintenance of
alveolar vertical bone height, bone density, and the
osseointegration course following the insertion of
titanium implants.
Materials and methods
Surgical procedures
Twenty-four adult laboratory male rabbits
(Oryctolagus cuniculus), 6 months-old, weighing
between 3 and 4 kg were used for this study. All experiments
were carried out in accordance with the
European Communities Council Directive of
November 24, 1986 (86/609/EEC) regarding the care
and use of animals for experimental procedures, and
were approved by the Institutional Review Board of
Bauru Dental School, University of Sa˜o Paulo.
During the experiment the animals were put in individual
cages with specific breed and water ad libitum.
Each animal was anesthetized (ketamine hydrochloride
50 mg/kg and xylazine hydrochloride 5 mg/kg) and
underwent routine oral disinfection procedures, which
included tongue cleaning, irrigation, and rinsing with
chlorhexidine before the surgical extraction of both
bilateral lower incisors. Due to the incisive anatomy,
one 4 mm-diameter defect distally, communicating
with each alveolar socket was performed.
Next, one of the sockets, chosen at random, was
completely filled with a bovine derived cancellous inorganic
bone graft in particles of 0.5–0.75mm with slow
resorption rate (Gen-ox , BAUMER SA, Mogi Mirim,
SP, Brazil), whereas the remaining socket became filled
with blood before being closed by continuous suture.
Post-operatory medication consisted in intramuscular
injection of analgesic (ketoprofen 1 mg/kg) for 3 days
and antibiotic (tetraciclin 25 mg/kg) at the procedure
day and after 7 days.
Sixty days after the first procedures, the rabbits were
prepared for surgical insertion of 3.75 8.5mm
machined surface titanium implants (Conexa˜o
Implantes, Aruja´ , SP, Brazil) at the previously exposed
areas of the mandible (right and left sides). This size
was chosen due to the limited vertical and horizontal
rabbit’s mandible bone thickness. Under abundantly
cooled sterile saline irrigation, a guide drill was first
used to mark the implant locations. The sites were
then sequentially enlarged to 2 and 3mm in diameter
with spiral drills and were finally tapped. Post-implants
radiographs were performed to verify the implant position
(Figure 1).
After implantation, on days 0, 30, 60, and 180, six
animals of each group were killed by overdose of anesthetics
and intra-cardiac injection of potassium chloride.
The respective mandibles were immediately
removed and split in half at the mental symphysis
before being fixed in 10% neutral buffered
formaldehyde.
Radiographic evaluation
Each hemi-mandible was positioned on the sensor of
the periapical radiographic digital system (Digora,
Soredex Orion Corporation, Helsinki, Finland) using
the paralleling technique with RINN XCP positioner
(Dentsply, Elgin, Illinois, USA) and exposed to X-rays
(X-707, Yoshida Dental MFC Co. Ltd, Tokyo, Japan,
set at 70 kVp, 7 mA) with a focus–film distance of 40 cm
in a parallel direction for 0.09 s.
The evaluation of the radiographic images was
performed using Digora software (Orion Co. Soredex,
Helsinki, Finland) (Figure 2).
Figure 1. Post-implant radiograph showing adequate implant
position.
2 Journal of Biomaterials Applications 0(0)
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The mean distance from the alveolar bone crest to
the implant platform (vertical bone height) was
obtained from the mesial and distal implant sides,
whereas the mean radiographic bone density (pixel
value) was measured in four areas adjacent to the
implant (two mesial and two distal).
Histological and morphometrical assessment
The specimens were dehydrated using an ascending
series of ethanol, embedded in glycolmethacrylate
(Technovit 7200 s, Heraeus Kulzer GmbH, Wehrheim,
Germany) and polymerized. Undecalcified sections of
200–300 mm were obtained in the long axis of the
implants (longitudinal), perpendicular to their threads
using Exakt Cutting-Grinding System (EXAKT
Apparatus GmbH, Norderstedt, Germany). On regular
pauses, each implant platform was measured with a
digital caliper and when the maximum diameter of
the titanium screw was confirmed (3.75 mm) at one
side, the other was successively ground to a thickness
between 70 and 100 mm, so that tissue assessment halfway
implant buccal and lingual edge could be
performed. Since de greatest part each embedded specimen
had to be grinded, just a single section could be
obtained from each specimen. Afterwards, the sections
were stained with toluidine blue 1%. Microscopically it
can be observed in all sections soft tissue of the oral
mucosa, connective tissue, and mature bone around the
threads and also biomaterial particles in experimental
group. The mature bone evidences major trabeculae
with Harversian canals and filling cones, characteristics
of bone turnover (Figures 3 and 4).
A single blind examiner performed the histometric
analysis using an image analysis system consisting of a
Zeiss Axioskop 2 microscope, Sony CCDIRIS- RGB
camera (Sony Corporation, Tokyo, Japan) and
Kontron KS-300 software (Kontron Elektronik
GmbH, Image Analysis Division, Echinf, Munich,
Germany) connected to an IBM computer, using 10
and 40 objectives.
One section representative of the implant
mid-portion was used. Due to the semi-circle format
of the rabbit’s socket, only the apical portion of the
titanium implant had certain contacted the xenograft
despite the defect performed, so the three apical titanium
threads at both sides (mesial and distal) were
selected as interest area. The digital images of three
apical titanium threads adjacent to the mesial and
distal sides of implant were obtained and the percentage
of bone-to-implant contact (BIC) defined as the
length of bone surface border in direct contact with
the implant perimeter, as well as the percentage of
bone area (BA) within the limits of the implant threads
were evaluated.
The resulting mean value of these measurements was
then used for statistical calculations.
Statistical analysis
The method of Kolmogorov and Smirnov was
used to confirm that the data were sampled from
Figure 2. Radiographic image measured on Digora Software.
Munhoz et al. 3
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a Gaussian distribution. After, the data were analyzed
with a misted two-factor analysis of variance
(ANOVA) for comparisons among time intervals and
individual comparisons between groups were executed
by means of paired t-test both adjusted to the 95%
confidence interval. Statistical analyses were performed
with SPSS software v.18 0 for windows (SPSS,
Chicago, IL, USA)
Results
Radiographic analysis
The crest to implant distances in the experimental and
control groups were not statistically different in the
intervals studied. In paired t-test there was a statistical
difference in radiographic density between the experimental
and control groups in all the time intervals, the
experimental group being higher (p¼0.0004 at day 0,
p¼0.0030 at 30 days, p¼0.0151 at 60 days, and
p¼0.0002 at 180 days).
When the time intervals were compared, the radiographic
crest to bone distances and bone density were
not statistically different (Table 1).
Histological and morphometric findings
The medullar space was occupied by bone marrow
tissue. All implants in the two groups appeared to be
osseointegrated, that is showed no soft-tissue encapsulation.
No major morphologic differences were seen
among the three groups in the cortical bone and
marrow tissues. Both endosteal and periosteal bone
proliferation was noted in all groups. The bone
Figure 3. Representative histological view of wound healing around implant in the control and experimental groups at days 0, 30, 60,
and 180. Direct bone to implant contact with some connective tissue and the presence of the biomaterial is shown. (TB stain, original
magnification 10).
Figure 4. Representative histological view of socket healing in
the experimental group. Direct interaction of the biomaterial and
bone with the presence of osteoblasts (!) and filling cones can
be observed. (TB stain, original magnification 40).
4 Journal of Biomaterials Applications 0(0)
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apposition was evaluated observing bone trabeculae
volume and the presence of filling cones.
In the control group at all periods the mature bone
marrow was in direct contact with the implant and
some connective tissue, while in the experimental
group the biomaterial (inorganic bovine graft) was in
contact with the adjacent bone and eventually with the
implant, and there was some adjacent connective tissue
(Figure 3). In all time intervals, the biomaterial had
direct interaction with the adjacent bone without
fibrous encapsulation (Figure 4).
The results are summarized in Table 2. In two-way
ANOVA test there was no significant difference in the
BIC through the intervals (p¼0.1196) in the experimental
group, but in the control group there were
differences between days 0 and 60 (p¼0.0013) and
days 0 and 180 (p¼0.0039). At paired t-test the experimental
group showed significantly higher values of
BIC on day 0 compared to the control group
(p¼0.0117) and there was no difference in the other
periods (p¼0.2370 at 30 days, p¼0.6414 at 60 days,
and p¼0.7353 at 180 days).
In two-way ANOVA test the differences in BA
throughout the intervals were not statistically significant
for the control and experimental groups
(p¼0.2556). There were no significant differences in
BA detected between the control and experimental
groups in paired t-test (p¼0.1132 on day 0,
p¼0.1329 at 30 days, p¼0.9659 at 60 days, and
p¼0.2111 at 180 days).
Discussion
For clinical diagnosis, radiographic analysis is the only
objective method available for implant/graft interaction
assessment, and the ideal methods of biomechanical
and microscopy analysis are nearly unfeasible.
The criteria normally adopted to determine implant
success through radiographic analysis are the absence
of continuous radiolucency around the implant14 and
the extent of vertical bone loss, which should not
exceed 0.9mm to 1.6mm during the first year and
0.2mm in the subsequent years.13,14
When the vertical bone loss index of the control
specimens were summed throughout the tested intervals,
the total level of loss was higher than the standard
established, but similar to that presented by Hatley
et al.15 for bone regression in rabbit tibias.
The absence of significant differences in the crest to
bone distance between the experimental and control
groups, during the whole period of the experiment,
suggested that the xenograft did not promote vertical
alterations in bone height after the insertion of titanium
implants. Although this method of measurement is
routinely used as a parameter for bone healing assessment
executed after tooth extraction, periodontal treatment
and implant insertion,8,14,15–19 in this study VBH
results of the experimental group might not be relevant
for this purpose because the grafted area around the
implant was too tiny and thus not adequately plausible
for assumptions. The small buccolingual thickness of
Table 1. Data from the radiographic analysis of vertical bone height and bone density.
Periods
Vertical bone height (mm) Bone density (pixel value)
Control Experimental Control Experimental
Initial (day 0) 0.2625 0.27 0.6958 0.73 162.49 3.59a 182.78 7.79a
30 days 1.3833 2.27 1.4375 0.95 163.69 14.71b 187.07 5.18b
60 days 0.225 0.21 0.9041 1.08 160.14 17.50c 184.41 4.68c
180 days 1.016 1.79 1.5708 1.91 144.13 5.67d 181.66 10.66d
a,b,c,dStatistically significant (p 0.05).
Table 2. Data form the histomorphometrical analysis of bone implant contact (BIC) and bone mass (BM).
BIC (%) BM (%)
Periods Control Experimental Control Experimental
Initial (day 0) 36.32 11.25abc 70.31 23.02c 39.19 11.31 64.58 27.76
30 days 58.18 18.95 70.91 13.08 43.72 12.37 53.63 12.37
60 days 73.75 16.10a 69.98 21.68 54.94 18.27 55.43 18.27
180 days 69.43 9.42b 65.46 19.54 62.97 21.20 50.62 21.20
a,b,cStatistically significant (p 0.05).
Munhoz et al. 5
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rabbit’s mandible limits the creation of wider experimental
bone defects, thus even the thinnest implant
screws available provide a restricted space for graft
particles around the coronal and middle portion of
the titanium implants.
Moreover, some variation in the radiographic
distance of bone crest-to-implant shoulder (VBH) has
probably occurred since the adoption of more efficient
measures for correcting the unavoidable radiographic
distortion of the implant inserted into bone was not
feasible.
Radiographic density is positively correlated with
bone mineral deposition, and for this reason its assessment
may be used to estimate the extent of healing in
the bone adjacent to the implant.12,15,20 The difference
in radiographic bone density between groups after 180
days was already described in a clinical prospective
study using a third molar socket model.19 Possibly the
radiopacity provided by the mineral content of remaining
graft particles could explain this result. Similar findings
were described by Zitzman et al.,6 when an
analogue cancellous bovine bone-derived graft
(BioOssTM) was applied in humans and by Oltramari
et al.21 using a socket’s model in minipigs. The authors
also suggested that the inorganic part of the xenograft
particles may be resorbed after long periods; however in
this investigation, this hypothesis could not be
disproved.
Due to the semi-circle format of the rabbit’s socket,
only the apical portion of the titanium implant had
certain contacted the xenograft despite the defect
performed. Therefore, the degree of bone implant
contact was measured in both mesial and distal surfaces
of the last three threads of the screw (interest area); this
is a reliable procedure that is supported by other
investigations.13,22–28
The degree of bone-implant contact observed in this
study was comparable to the ones presented in other
studies using similar xenograft materials7,25 or higher
than that described by De Vicente et al.,23 Rahmani
et al.24 and Schwarz et al.26 The absence of significant
differences between groups when the bone-implant
contact mean values were assessed on days 30, 60,
and 180 of the experiment and the similarity to the
results of other investigations7,23–26 could indicate
that the presence of a bovine-derived inorganic graft
at the implant insertion area did not impair, at any
time, the titanium osseointegration.
The unexpected lower BIC observed in the
nongrafted controls at day 0 may be due to the characteristics
of rabbit’s osseous tissue, in other words the
expressive content of bone marrow, scanty bony trabeculae,
and the tiny cortical.29 Thus, during implant insertion
probably the inherent lower stiffness of this
structure resulted in cortical fragmentation in a way
that almost no contact of bone trabeculae to titanium
implant occurred. The fact that the experimental group
has a significantly higher BIC value at time 0 is an
important finding for the primary fixation of the
system and it can be explained by the presence of the
biomaterial that served as conductor to precocious
bone deposition at experimental sites and improved
the bone resistance.
Since bone healing went on through 180 days, no
difference in BIC was observed between groups at this
interval possibly because the inherent increase in bone
trabeculae quantity surrounding the implant in the
control group responded for this equivalence.
Our BA after 180 days results were equivalent to the
results presented by De Vicente et al.23 who used a
similar graft material (BioOssTM) in the mandibles of
dogs. However, the general BA detected in the xenograft
group was higher than that observed by Schwartz
et al.,26 who used an analogue material (BioOssTM).
Although both products were bovine derived cancellous
inorganic bone grafts and presented similar chemical
and physical properties,30 fortuitous differences in
manufacturing procedure and formula should be
taken into account.
Given the absence of significant modifications in the
BA, BIC, and BD of the experimental group from 30 to
180 days, it could be suggested that the microscopic
response of medullar mandible bone of rabbits to the
titanium implant is established in the first 30 days.
Since it is the first study to use inorganic bovine graft
associated to titanium implants at rabbit’s mandible
site, periods of 30, 60, and 180 days were performed
because there is not literature data to preview in
how much time there was osseointegration on this
grafted area.
From the initial sample of 28 animals, four presented
infection at the implantation possibly by contamination
or surgical technique error, as described by Montes
et al.31 Although those animals were discarded, the
factors may have had some influence on measured
pieces/data obtained thus being responsible for an
increase in variance (Tables 1 and 2) and the lack of
statistical difference between groups.
Clinicians should know that inorganic bovine xenograft
following tooth extraction may be a practical and
viable option to avoid an unnatural appearance of the
final crown resulting from irregular ridge anatomy after
bone remodeling. Apart from maintaining alveolar
bone architecture or providing bone gain, observed in
recent follow-up researches,10,32,33 grafting with inorganic
xenograft seems not interfere with implant
osseointegration. It should be clear; however, that the
procedures tested in combination may not be applicable
to humans and before this occurs, more specific studies
are necessary.
6 Journal of Biomaterials Applications 0(0)
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Conclusion
Under the conditions of this prospective study, it can be
concluded that the use of an inorganic xenograft prior
to a titanium implant insertion did not interfere with
the course of osseointegration of titanium implants in
rabbit’s mandible.
Acknowledgments
The authors disclose any conflicts of interest. Baumer SA and
Conexa˜o Sistema de Pro´ teses Ltda kindly donated the inorganic
bovine bone and implant screws used, respectively. The
authors wish to thank FAPESP process 06/1545-7 for providing
funds for this research and to American Journal Experts
for English editing service.
References
1. Camargo PM, Lekovic V, Weinlaender M, et al.
Influence of bioactive glass on changes in alveolar process
dimensions after exodontia. Oral Surg Oral Med Oral
Pathol Oral Radiol Endod 2000; 90: 581–586.
2. Carmagnola D, Adriaens P and Berglundh T. Healing of
human extraction sockets filled with Bio-Oss. Clin Oral
Impl Res 2003; 14: 137–143.
3. Artzi Z, Tal H and Dayan D. Porous bovine bone mineral
in healing of human extraction sockets: 2.
Histochemical observations at 9 months. J Periodontol
2001; 72: 152–159.
4. Benke D, Olah A and Mohler H. Protein-chemical analysis
of Bio-Oss bone substitute and evidence on its carbonate
content. Biomaterials 2001; 22: 1005–1012.
5. Piattelli M, Favero GA, Scarano A, Orsini G and Piattelli
A. Bone reactions to anorganic bovine bone (Bio-Oss)
used in sinus augmentation procedures: a histologic
long-term report of 20 cases in humans. Int J Oral
Maxillofac Implants 1999; 14: 835–840.
6. Zitzmann NU, Scharer P, Marinello CP, Schupbach P
and Berglundh T. Alveolar ridge augmentation with
Bio-Oss: A histological study in humans. Int J Period
Rest Dent 2001; 21: 289–295.
7. You TM, Choi BH, Li J, et al. The effect of platelet-rich
plasma on bone healing around implants placed in bone
defects treated with Bio-Oss: a pilot study in the dog
tibia. Oral Surg Oral Med Oral Pathol Oral Radiol
Endod 2007; 103: e8–e12.
8. Meijndert L, Raghoebar GM, Meijer HJA and Vissink A.
Clinical and radiographic characteristics of single tooth
replacements preceded by local ridge augmentation: a
prospective randomized-clinical trial. Clin Oral Impl Res
2008; 19: 1295–1303.
9. Meijndert L, Raghoebar GM, Schupbach P, Meijer HJA
and Vissink A. Bone quality at the implant site after
reconstruction of a local defect of the maxillary anterior
ridge with chin bone or deproteinised cancellous bovine
bone. Int J Oral Maxillofac Surg 2005; 34: 877–884.
10. Ferreira CE, Novaes AB, Haraszthy VI, Bittencourt M,
Martinelli CB and Luczyszyn SM. A clinical study of 406
sinus augmentations with 100% anorganic bovine bone.
J Periodontol 2009; 80: 1920–1927.
11. Buser D, Weber HP and Lang NP. Tissue integration of
non-submerged implant 1-year results of a prospective
study with 100 ITI hollow-cylinder and hollowscrew
implants. Clin Oral Implan Res 1990; 1: 33–40.
12. Bragger U. Radiographic parameters for the evaluation
of peri-implant tissues. Periodontology 2000; 4: 87–97.
13. Albrektsson T, Zarb G, Worthington P and Eriksson
AR. The long-term efficacy of currently used dental
implants: a review and proposed criteria of success. Int
J Oral Maxillofac Implants 1986; 1: 11–25.
14. Albrektsson T and Isidor F. Consensus report of
session IV. In: Lang NP, Karring T (eds) Proceedings
of the 1st European Workshop on Periodontology.
London: Quintessence Publishing Co. Ltd, 1994,
pp.365–369.
15. Hatley CL, Cameron SM, Cuenin MF, Parker MH,
Thompson SH and Harvey SB. The effect of dental
implant spacing on peri-implant bone using the rabbit
(Oryctolagus cuniculus) tibia model. J Prosth 2001; 10:
154–159.
16. Choi CR, Yu HS, Kim CH, et al. Bone cell responses of
titanium blasted with bioactive glass particles. J Biomater
App 2010; 25: 99–117.
17. Blanes RJ, Bernard JP, Blanes ZM and Belser UC. A
10-year prospective study of ITI dental implants placed
in the posterior region. I: Clinical and radiographic
results. Clin Oral Impl Res 2007; 18: 699–706.
18. Kim DM, Badovinac RL, Lorenz RL, Fiorellini JP and
Weber HP. A 10-year prospective clinical and radiographic
study of one-stage dental implants. Clin Oral
Impl Res 2008; 19: 254–258.
19. MunhozEA, Ferreira Junior O, YaeduRYF and Granjeiro
JM. Radiographic assessment of impacted mandibular
third molar sockets filled with composite xenogenic bone
graft. Dentomaxillofacial Radiol 2006; 35: 371–375.
20. Dodds RA, York-Ely AM, Zhukauskas R, et al.
Biomechanical and radiographic comparison of demineralized
bone matrix, and a coralline hydroxyapatite in a
rabbit spinal fusion model. J Biomater Appl 2010; 25:
195–215.
21. Oltramari PV, Navarro Rde L, Henriques JF, et al.
Evaluation of bone height and bone density after tooth
extraction: an experimental study in minipigs. Oral Surg
Oral Med Oral Pathol Oral Radiol Endod 2007; 104:
e9–16.
22. Balatsouka D, Gotfredsen K, Lindh CH and Berglundh
T. The impact of nicotine on bone healing and osseointegration.
An experimental study in rabbits. Clin Oral Impl
Res 2005; 16: 268–276.
23. De Vicente JC, Recio O, Martı´n-Villa L, Junquera LM
and Lo´ pez-Arranz JS. Histomorphometric evaluation of
guided bone regeneration around implants with SLA surface:
an experimental study in beagle dogs. Int J Oral
Maxillofac Surg 2006; 35: 1047–1053.
24. Rahmani M, Shimada E, Rokni S, et al. Osteotome sinus
elevation and simultaneous placement of porous-surfaced
dental implants: a morphometric study in rabbits. Clin
Oral Impl Res 2005; 16: 692–699.
Munhoz et al. 7
Downloaded from jba.sagepub.com at UNIV DE SAO PAULO BIBLIOTECA on June 30, 2011
25. Therheyden H, Jepsen S, Mo¨ ller B, Tucker MM and
Rueger DC. Sinus floor augmentation with simultaneous
placement of dental implants using a combination
of deproteinized bone xenogenic and recombinant
human osteogenic protein-1. A histometric study in
miniature pigs. Clin Oral Implant Res 1999; 10:
510–521.
26. Schwarz F, Rothamel D, Herten M, et al.
Immunohistochemical characterization of guided bone
regeneration at a dehiscence-type defect using different
barrier membranes: an experimental study in dogs.
Clin Oral Impl Res 2008; 19: 402–415.
27. Nikolidakis D, Meijer GI, Oortgiesen DAW,
Walboomers XF and Jansen JA. The effect of a low
dose of transforming growth factor b1 (TGF-b1) on the
early bone-healing around oral implants inserted in trabecular
bone. Biomaterials 2009; 30: 94–99.
28. Veis AV, Trisi P, Papadimitriou S, et al. Osseointegration
of Osseotites and machined titanium implants in
autogenous bone graft. A histologic and histomorphometric
study in dogs. Clin Oral Impl Res 2004; 15: 54–61.
29. Cordioli G, Atiyeh F, Piattelli A and Majzoub Z. Healing
of transplanted composite bone grafts–implants: a pilot
animal study. Clin Oral Implan Res 2003; 14: 750–758.
30. Accorsi-Mendonc¸a T, Conz MB, Barros TC, de Sena LA,
Soares Gde A and Granjeiro JM. Physicochemical characterization
of two deproteinized bovine xenografts. Braz
Oral Res 2008; 22: 5–10.
31. Montes CC, Pereira FA, Thome´ G, et al. Failing factors
associated with osseointegrated dental implant loss.
Implant Dent 2007; 16: 404–412.
32. Arau´ jo M, Linder E, Wennstro¨m J and Lindhe J. The
influence of bio-oss collagen on healing of an extraction
socket: an experimental study in the dog. Int J Period
Rest Dent 2008; 28: 123–135.
33. Arau´ jo MG and Lindhe J. Ridge preservation with the
use of Bio-Osss collagen: a 6-month study in the dog. Clin
Oral Impl Res 2009; 20: 433–440.
8 Journal of Biomaterials Applications 0(0)
Downloaded from jba.sagepub.com at UNIV DE SAO PAULO BIBLIOTECA on June 30, 2011

Immediately loaded titanium implant with a tissue-stabilizing/maintaining design (‘beyond platform switch’) retrieved from man after 4 weeks: a histological and histomorphometrical evaluation. A case report


Marco Degidi
Giovanna Iezzi
Antonio Scarano
Adriano Piattelli
Authors’ affiliations:
Marco Degidi, Giovanna Iezzi, Antonio Scarano,
Adriano Piattelli, Dental School, University of
Chieti-Pescara, Chieti, Italy
Marco Degidi, Private Practice, Bologna, Italy
Correspondence to:
Prof. Adriano Piattelli, MD, DDS
Via F. Sciucchi 63
66100 Chieti
Italy
Tel.:þ00 39 0871 3554083
Fax:þ00 39 0871 3554076
e-mail: apiattelli@unich.it
Key words: conical abutment connection, crestal bone remodeling, dental implants,
histology, immediate loading, microgap, Morse cone connection, platform switching
Abstract
Background: After implant insertion and loading, crestal bone usually undergoes
remodeling and resorption. If the horizontal relationship between the outer edge of the
implant and a smaller-diameter component (‘platform switching’) is altered, there seems to
be reduced crestal bone loss. Immediate loading allows immediate restoration of esthetics
and function, reduces morbidity, and facilitates functional rehabilitation.
Materials and methods: Three Morse cone connection implants were inserted in the right
posterior mandible in a 29-year-old partially edentulous patient. The platform of the
implant was inserted 2mm below the level of the alveolar crest. After a 1-month loading
period, the most distal mandibular implant was retrieved with a trephine bur for
psychological reasons.
Results: At low-power magnification, it was possible to see that bone was present 2mm
above the level of the implant shoulder. No resorption of the coronal bone was present. No
infrabony pockets were present. At the level of the shoulder of the implant, it was possible
to observe the presence of dense connective tissue with only a few scattered inflammatory
cells. Newly formed bone was found in direct contact with the implant surface. The bone–
implant contact percentage was 65.3 4.8%.
Conclusions: Abutments smaller than the diameter of the implant body (platform
switching) in combination with an absence of micromovement and microgap may protect
the peri-implant soft and mineralized tissues, explaining the observed absence of bone
resorption. Immediate loading did not interfere with bone formation and did not have
adverse effects on osseointegration.
Stable crestal bone levels are believed to be
critical for the long-term implant success
(Chou et al. 2004). After implant insertion
and loading, crestal bone usually undergoes
remodeling and resorption during the first
year following prosthetic restoration, in
two-piece implants (Hermann et al.
2000a). Crestal bone levels have been reported
to be usually located about 1.5–
2mm below the implant–abutment junction
(IAJ) after 1 year following implant
restoration (Lazzara & Porter 2006).
Cochran et al. (1997) and Hermann et al.
(1997, 2000b, 2001) demonstrated that
crestal bone remodels to a level about
2.0mm apical to the IAJ. Several hypotheses
have been offered to explain this remodeling.
Some investigators have related
this remodeling to a stress concentration
at the crestal level, while others believe
that the presence of a microgap and possible
microleakage and micromovement
Date:
Accepted 15 January 2007
To cite this article:
Degidi M, Iezzi G, Scarano A, Piattelli A. Immediately
loaded titanium implant with a tissue stabilizing/
maintaining design (‘beyond platform switch’) retrieved
from man after 4 weeks: a histological and
histomorphometrical evaluation. A case report.
Clin. Oral Impl. Res. 19, 2008; 276–282
doi: 10.1111/j.1600-0501.2007.01449.x
276 c 2007 The Authors. Journal compilation c 2007 Blackwell Munksgaard
could lead to a localized inflammation of
the peri-implant soft tissues (Quirynen &
Van Steenberghe 1993; Quirynen et al.
1994; Persson et al. 1996; Cochran et al.
1997; Hermann et al. 1997, 2000a, 2001;
Jansen et al. 1997; Misch et al. 2001;
Piattelli et al. 2001, 2003). The potential
influence of implant design on peri-implant
bone loss warrants additional research
(Chou et al. 2004). The loss of
crestal bone has also been reported to be
influenced by the relationship of the IAJ
to the crestal bone (Chou et al. 2004).
Hermann et al. (2001) and Piattelli et al.
(2003) have demonstrated that when the
IAJ is positioned deeper within the bone,
the resulting loss of vertical crestal bone
height increases.
When a matching implant–abutment
diameter is used, the inflammatory cell
infiltrate (abutment ICT) is located at the
outer edge of the IAJ close to crestal bone;
this close proximity may explain partially
the biologic and radiographic observations
of crestal bone loss around restored twopiece
implants (Lazzara & Porter 2006).
On the other hand, if the horizontal relationship
between the outer edge of the
implant and a smaller-diameter component
(‘platform switching’) is altered in addition
to other favorable implant design conditions,
there seems to be a reduced crestal
bone loss (Lazzara & Porter 2006). This
fact could be explained by an increased
surface area created by the exposed implant
seating surface with a reduction in the
quantity of crestal bone resorption needed
to expose a minimal amount of implant
surface to which the soft tissues can attach
(Lazzara & Porter 2006). Furthermore, the
internal repositioning of the IAJ away from
the external, outer edge of the implant and
neighboring bone decreases the effects of
the abutment ICT on surrounding tissues
(Abrahamsson et al. 1998; Lazzara &
Porter 2006). The reduced exposure and
confinement of the platform-switched
abutment ICT may result in a reduced
inflammatory effect (Lazzara & Porter
2006). Additonally, the exposed horizontal
part of the implant shoulder was also microroughened,
and this enhances the
chance of bone growth on top of this
surface.
A Morse cone connection implant (Ankylos
s, Dentsply-Friadent) has an in-built
beyond platform switching and was designed
with, among others, the following
objectives:
(1) it should allow for optimum load distribution
for permanent load stability
during functional loading;
(2) it should facilitate soft-tissue stability
due to the gap-free bacteria-proof tapered
abutment connection withmaximum
mechanical stability and the
lack of any micromovement (Nentwig
2004).
In a previous histological report of an
immediately loaded Morse cone connection
implant, retrieved from man after a
6-month loading period, we reported the
presence of newly formed bone trabeculae
at the most coronal portion on one side of
the implant; these trabeculae were surrounded
by osteoblasts actively secreting
osteoid matrix with no osteoclasts present.
We thought that the presence of this newly
formed bone in the coronal peri-implant
area was striking and we hypothesized that
it could be related to the absence of a
microgap due to the conical connection
with no bacterial colonization and leakage
at the implant–abutment interface (Degidi
et al. 2004).
Photoelastic and finite element analysis
studies have shown that the special thread
design of this implant reduces the functional
stresses at the crestal bone compared
with other implant systems (Morris et al.
2004; Nentwig 2004). Load-induced cervical
bone loss occurred in o20% of cases,
and even in these cases, the amount of
crestal bone loss was minimal (Nentwig
2004).
In a study, in 50% of the cases, X-ray
examination after 1 year of prosthetic loading
showed crestal bone at or slightly above
the level of the implant shoulder (Doring
et al. 2004).
Chou et al. (2004), in a study of over
1500 Morse cone connection implants,
reported a total overall mean loss from
implant placement to 36 months postloading
of only 0.6 or 0.2mm/year, including
the bone loss that can be attributed to
surgical trauma.
Immediate loading of dental implants
was thought to produce a fibrous repair at
the interface (Bra°nemark et al. 1977; Adell
et al. 1981; Carter & Giori 1991; Brunski
1991, 1992). Several histological reports, in
man and experimental animals, have, on
the contrary, shown mineralized tissues at
the interface in early and immediately
loaded implants (Linkow et al. 1992;
Piattelli et al. 1993a, 1993b, 1997a,
1997b, 1997c, 1998; Trisi et al. 1993;
Ledermann et al. 1999; Romanos et al.
2001; Testori et al. 2001; Romanos et al.
2002; Testori et al. 2002; Rocci et al. 2003;
Siar et al. 2003; Degidi et al. 2004; Degidi
et al. 2005a, 2005b; Traini et al. 2005a,
2005b; Neugebauer et al. 2006). Immediate
loading allows immediate restoration of
esthetics and functions, reduces the morbidity
of a second surgical intervention, and
facilitates the functional rehabilitation increasing
patient acceptance and satisfaction.
There is a need to investigate the
bone healing processes at the interface,
especially regarding which type of bone
response is present around immediately
loaded implants inserted in poorer quality
bone (Degidi et al. 2005a, 2005c). An
analysis of human biopsies of immediately
loaded implants is the best way to ascertain
the quality and quantity of the peri-implant
hard tissues (Romanos et al. 2005). The
role that implant surfaces play, especially
on the early healing processes at the interface
is also important. A sandblasted and
acid-etched surface (Friadents plus surface,
Dentsply) was obtained with a novel gritblasting
and acid-etching technique and
showed a regular microroughness with
pores in the micrometer dimension overlaying
a macroroughness structure caused
by the grit blasting. (Papalexiou et al. 2004;
Rupp et al. 2004). The spatial architecture
showed a first level of roughness of
100 mm, a second level of grooves in the
dimensions of about 12–75 mm, each of
which embraced an arrangement of smaller
round-shaped groups with diameters of
about 1–5 mm (Papalexiou et al. 2004;
Rupp et al. 2004).
The aim of this study was to evaluate the
peri-implant soft and mineralized tissues
around an immediately loaded implant,
with a conical implant abutment connection,
after a 1-month loading period.
Materials and methods
Three Morse cone connection dental
implants (ANKYLOSs plus DENTSPLYFriadent,
Mannheim, Germany) were
inserted in the right posterior mandible in
Degidi et al . Human immediately loaded implant
c
2007 The Authors. Journal compilation c 2007 Blackwell Munksgaard 277 | Clin. Oral Impl. Res. 19, 2008 / 276–282
a 29-year-old partially edentulous patient.
The platform of the implants was inserted
2mm below the level of the alveolar crest,
1mm deeper than the manufacturer’s protocol
(Fig. 1). The patient was a heavy
smoker. All the implants were immediately
loaded with a provisional resin restoration
the same day of the implant
surgery. After a 1-month loading period,
the most distal mandibular implant was
retrieved with a 5.5-mm trephine bur for
psychological reasons (Fig. 2). The patient
had developed, almost immediately after
implant insertion, an aversion to this implant,
thought that it was causing an inflammation
that could lead to cancer
development, and psychological counseling
did not obtain any results. This implant
was a 3.5 8mm implant inserted in the
D3 bone with an insertion torque of
23.8Ncm. The ISQ value was 63 at
implant insertion and 66 before implant
retrieval.
Specimen processing
The implant and surrounding tissues were
washed in saline solution and immediately
fixed in 4% para-formaldehyde and 0.1%
glutaraldehyde in 0.15M cacodylate buffer al
4 C and pH 7.4. The specimen was processed
using the Precise 1 Automated
System (Assing, Rome, Italy). (Piattelli
et al. 1997d). The specimen was dehydrated
in an ascending series of alcohol
rinses and embedded in a glycolmethacrylate
resin (Technovit 7200 VLC, Kulzer,
Wehrheim, Germany). After polymerization
the specimen was sectioned along its
longitudinal axis with a high-precision diamond
disk at about 150 mm and ground
down to about 30 mm with a specially
designed grinding machine. Three slides
were obtained. These slides were stained
with acid fuchsin and toluidine blue and
examined with a transmitted light Leitz
Laborlux microscope (Leitz, Wetzlar,
Germany) and a Zeiss fluorescence microscope
(Zeiss, Go¨ttingen, Germany).
Histomorphometry of bone-implant contact
percentage was carried out using a light
microscope (Laborlux S, Leitz) connected
to a high-resolution video camera (3CCD,
JVC KY-F55B, JVCs, Yokohama, Japan)
and interfaced to a monitor and PC (Intel
Pentium III 1200 MMX, Intels, Santa
Clara, CA, USA). This optical system
was associated with a digitizing pad (Matrix
Vision GmbH, Oppenweiler, Germany)
and a histometry software package with
image-capturing capabilities (Image-Pro Plus
4.5, Media Cybernetics Inc., Immagini &
Computer Snc, Milano, Italy).
Results
At low-power magnification, it was possible
to see that bone was present 2mm
above the level of the implant shoulder
(Fig. 3). In the first three coronal mm it
was possible to observe the presence of
lamellar cortical compact bone around the
implant (Fig. 4). In this region, many areas
of bone remodeling were present; bone
remodeling units (BMU) were also present
(Fig. 5). Areas of new bone formation were
present, with osteoblasts depositing osteoid
matrix. A rim of osteoblasts lined the
marrow spaces found at the coronal level;
these osteoblasts were depositing osteoid
matrix. At the coronal level, osteoblasts
were also found in direct contact with the
implant surface; these osteoblasts were
laying down osteoid matrix directly on
the metal surface. No resorption of the
coronal bone was present. No infrabony
pockets were present. At the level of the
shoulder of the implant, it was possible to
observe the presence of a dense connective
tissue with only a few inflammatory cells.
Newly formed bone was found in direct
contact with the implant surface. No fibrous
connective tissue was found at the
bone–titanium interface. No epithelial
downgrowth was present. No active bone
resorption was present in the middle and
apical portion of the implant perimeter and
osteoclasts were absent. All the interthread
spaces were filled by newly formed bone
with a thickness of 100–300 mm; it was
possible to observe two lines of osteocytes.
These osteocytes had their longest axis
always parallel to the implant surface. In
some portions of the implant surface, osteoblasts
were depositing osteoid matrix.
Many wide marrow spaces with many
capillaries were present in the peri-implant
bone. The bone near the implant appeared
to be moremature than the bone found at a
distance. No inflammatory cell infiltrate
was found around the implant. In the
apical portion, osteoblasts and newly
formed bone were present. No osteoclasts
Fig. 1. Radiographic aspect of the implant.
Fig. 2. The retrieved implant. The arrows show the coronal portion of the bone.
Degidi et al . Human immediately loaded implant
278 | Clin. Oral Impl. Res. 19, 2008 / 276–282 c 2007 The Authors. Journal compilation c 2007 Blackwell Munksgaard
were present. Few marrow spaces were
observed directly on the implant surface.
The bone–implant contact percentage was
65.3 4.8%.
Discussion
Only a few histological evaluations of immediately
loaded implants retrieved from
humans have been reported in the literature
(Linkow et al. 1992; Piattelli et al.
1993a, 1997a, 1997c; Trisi et al. 1993;
Ledermann et al. 1999; Testori et al.
2001, 2002; Rocci et al. 2003, 2005; Degidi
et al. 2005a, 2005b, 2005c; Romanos et al.
2005; Traini et al. 2005a, 2005b).
In the present histologic study, the aim
was to focus mainly on two aspects of the
peri-implant tissues:
(1) the soft peri-implant tissues;
(2) the aspect and characteristics of the
mineralized bone at the interface.
Because the emergence area of the
shoulder region of this implant is considerably
less than that in other systems that
use conventional implant–abutment connections,
the shoulder is positioned subcrestally
into the bone to produce an
optimal emergence profile (Doring et al.
2004). Placement of the implant deeper
into the bone does not necessarily result
in complications of the soft and hard tissues
that have been reported for other
implant systems (Doring et al. 2004). In
fact, in the present specimen it was found
that the bone had not undergone any resorption
and was still located about 2mm
above the implant shoulder.
This could be due to the positive effects
of a favorable load transmission to the bone
via the special progressive threads of this
implant, to a stable internal-tapered abutment
connection with the absence of any
microgap (Nentwig 2004) or micromovement,
and, finally, to the presence of a
thick layer of soft tissues in the narrowed
neck of the smaller-diameter abutment
(Doring et al. 2004). This collar of soft
tissue, which has a wedge-shaped cross
section, and which was found to be composed
of thick, fibrous connective tissue
with few scattered inflammatory cells,
probably provides an additional protective
function to the peri-implant bone (Doring
et al. 2004). It must, moreover, be stressed
that in this case the implants were inserted
in the posterior mandible and, probably,
the width of the ridge positively influenced
the histological result. Also the interimplant
distance was found to be a relevant
factor on crestal bone resorption. Tarnow
et al. (2000) found that the crestal bone loss
was lower for implants with a 43mm
distance between them. It can be hypothesized
that the present results would have
Fig. 4. At higher magnification, at the coronal level a rim of osteoblasts was producing osteoid matrix. Acid
fuchsin–toluidine blue. Figure on the left side magnification 50. Figure on the upper right side 100.
Figure on the right lower side 100.
Fig. 3. Immediately loaded Morse cone connection implant, inserted in the posterior mandible and retrieved
after 4 weeks. Low-power magnification on the left side. The bone–implant contact percentage was 65%. At
higher magnification, on the upper right side it was possible to see a rim of osteoblasts lining the marrow spaces
found at the coronal level: these osteoblasts were depositing osteoid matrix. At the coronal level, osteoblasts
were also found in direct contact with the implant surface: these osteoblasts were laying down osteoid
matrix directly on the metal surface. On the lower right side it was possible to observe a dense, fibrous
connective tissue with a few scattered lymphocytes. Acid fuchsin–toluidine blue. Figure on the left-side
magnification 12. Figure on the upper right-side 50. Figure on the right lower side 50.
Degidi et al . Human immediately loaded implant
c
2007 The Authors. Journal compilation c 2007 Blackwell Munksgaard 279 | Clin. Oral Impl. Res. 19, 2008 / 276–282
been different if the implants had been
placed closer together.
The surface characteristics of an implant
are important in determining the pattern of
healing under loading, especially in particularly
demanding situations such as immediate
loading.
The histological data obtained from the
present study confirm that immediate
loading did not have an adverse effect on
osseointegration, and the early bone healing
was not disturbed by the stresses transmitted
at the interface even if the implant
had been inserted in soft bone (D3). The
very high bone-to-implant contact percentage
found in the present implant (about
65%) after a healing period of only 4 weeks
is striking. This fact could be explained by
the microstructure of this surface that has
been shown to have a hierarchical surface
structure due to surface-modifying blasting
and etching processes, resulting in a wettable
surface (Rupp et al. 2004). This unique
wettability characteristic has been
hypothesized to determine an increased
adhesion to this surface of non-collagenous
proteins like sialoprotein and osteopontin,
which are the forerunners of contact osteogenesis
(Rupp et al. 2004). Moreover,
higher adsorbed amounts of fibronectin
may improve host responses such as osteoblast
adhesion (Rupp et al. 2004). At last,
the three-dimensional fibrin grid found on
this surface could produce a more favorable
structure for the in vivo three-dimensional
movement (from bone-to-implant surface)
of osteogenic differentiating cells (Di Iorio
et al. 2005).
Rocci et al. (2003) reported very high
bone–implant contact, (84.2%), with apparent
undisturbed healing in implants that
had been inserted in bone quality sites 3 or
4 and that had been biomechanically challenged.
The present results, moreover, confirm
those reported by Testori et al. (2002).
Immediately loaded splinted implants inserted
in the posterior mandible can osseointegrate
with a peri-implant response
similar to that of delayed loaded implants.
(Degidi et al. 2004, 2005a, 2005b,
2005c).
Conclusion
The use of an abutment smaller than the
diameter of the implant body (‘platform
switching’) can help to protect the periimplant
mineralized tissues. This fact
could, probably, partially explain the absent
or reduced rate of bone resorption
reported for this type of implant connection,
and observed in the present histological
case report.
The bacteria-proof seal, the lack of micromovements
due to the friction grip, and
the minimally invasive second-stage surgery
without any major trauma for the
periosteal tissues are also important factors
in preventing the cervical bone loss.
(Morris et al. 2004; Nentwig 2004). The
platform-switching concept most probably
could have a significant impact on the
implant treatment in esthetic areas. Care
should be taken in extrapolating the results
provided in this paper to the esthetic zone.
The present results show that a high
percentage of bone contact can be obtained
even in immediately loaded implants inserted
in soft bone, after a very short healing
period (4 weeks). Immediate loading did not
interfere with bone formation and did not
have adverse effects on osseointegration.
Acknowledgements: This work was
partially supported by the National
Research Council (C.N.R.), Rome, Italy,
by the Ministry of Education,
University, and Research (M.I.U.R.),
Rome, Italy, and by AROD (Research
Association for Dentistry and
Dermatology), Chieti, Italy.
References
Abrahamsson, I., Berglundh, T. & Lindhe, J. (1998)
Soft tissue response to plaque formnation at
different implant systems. A comparative study
in the dog. Clinical Oral Implants Research 9:
73–79.
Adell, R., Lekholm, U., Rockler, B. & Bra°nemark,
P-I. (1981) A 15 year study of osseointegrated
implants in the treatment of the edentulous
jaw. International Journal of Oral Surgery 10:
387–416.
Bra°nemark, P.I., Hansson, B.O., Adell, R., Breine,
U., Lindstrom, J., Halle´n, O. & Ohman, A.
(1977) Osseointegrated implants in the treatment
of the edentulous jaw. Experience from
a 10-year period.. Scandinavian Journal of
Fig. 5. Highermagnification of the areas (a and b) at the interface shown in Fig. 3.Woven bonewas observed in
direct contact with the implant surface; no gaps or connective tissue were present at the bone–implant
interface. Newly formed bone was present in the concavities of all threads of the implant. No fibrous
connective tissue was found at the bone–metal interface. No epithelial downgrowth was present. No active
bone resorptionwas present in this region, and the osteoclasts were absent. No inflammatory cell infiltratewas
present around the implant. Acid fuchsin–toluidine blue. Figure on the right side 100. Figure on the left
side 100.
Degidi et al . Human immediately loaded implant
280 | Clin. Oral Impl. Res. 19, 2008 / 276–282 c 2007 The Authors. Journal compilation c 2007 Blackwell Munksgaard
Plastic and Reconstructive Surgery 11 (Suppl. 16):
1–132.
Brunski, J.B. (1991) Influence of biomechanical
factor at the bone-biomaterial interface. In: Davies,
J.E., ed. The Bone–Biomaterial Interface,
391–405. Toronto: Toronto University Press.
Brunski, J.B. (1992) Forces on dental implants and
interfacial stress transfer. In: Laney, W.R. & Tolman,
D.E., eds. Tissue Integration in Oral,
Orthopaedic and Maxillofacial Reconstruction,
108–124. Chicago: Quintessence.
Carter, D.R. & Giori, N.J. (1991) Effect of mechanical
stress on tissue differentiation in the bony
implant bed. In: Davies, J.E., ed. The Bone–
Biomaterial Interface, 367–379. Toronto: University
of Toronto Press.
Cochran, D.L., Hermann, J.S., Schenk, R.K., Higginbottom,
F.L. & Buser, D. (1997) Biologicwidth
around titanium implants. A histometric analysis
of the implanto-gingival junction around unloaded
and loaded nonsubmerged implants in the canine
mandible. Journal of Periodontology 68: 186–98.
Chou, C.T., Morris, H.F., Ochi, S., Walker, L. &
DesRosiers, D. (2004) AICRG, Part II: crestal
bone loss associated with the Ankylos implant–
loading to 36 months. Journal of Oral Implantology
30: 134–143.
Degidi, M., Scarano, A., Piattelli, M. & Piattelli, A.
(2004) Histologic evaluation of an immediately
loaded titanium implant retrieved from a human
after 6 months in function. Journal of Oral Implantology
30: 289–296.
Degidi, M., Scarano, A., Piattelli, M., Perrotti, V. &
Piattelli, A. (2005a) Bone remodeling in immediately
loaded and unloaded titanium implants: a
histologic and histomorphometric study in man.
Journal of Oral Implantology 31: 18–24.
Degidi, M., Scarano, A., Iezzi, G. & Piattelli, A.
(2005b) Histologic and histomorphometric analysis
of an immediately loaded implant retrieved
from man after 14 months of loading. Journal of
Long Term Effects of Medical Implants 15: 489–
498.
Degidi, M., Scarano, A., Iezzi, G. & Piattelli, A.
(2005c) Histologic analysis in man of an immediately
loaded implant retrieved after 8 weeks.
Journal of Oral Implantology 31: 247–254.
Di Iorio, D., Traini, T., Degidi, M., Caputi, S. &
Piattelli, A. (2005) Blood clot organization on
different implant surfaces in man: an in vitro
study. Journal of Biomedical Materials Research
Part B: Applied Biomaterials 74B: 636–642.
Doring, K., Eisenmann, E. & Stiller, M. (2004)
Functional and esthetic considerations for singletooth
Ankylos implant-crowns: 8 years of clinical
performance. Journal of Oral Implantology 30:
198–209.
Hermann, J.S., Buser, D., Schenk, R.K. & Cochran,
D.L. (2000a) Crestal bone changes around titanium
implants. A histometric evaluation of unloaded
non-submerged and submerged implants in
the canine mandible. Journal of Periodontology
71: 1412–1424.
Hermann, J.S., Buser, D., Schenk, R.K., Higginbottom,
F.L. & Cochran, D.L. (2000b) Biological
width around titanium implants. A physiologically
formed and stable dimension over time.
Clinical Oral Implants Research 11: 1–11.
Hermann, J.S., Cochran, D.L., Nummikoski, P.V.
& Buser, D. (1997) Crestal bone changes around
titanium implants: a radiographic evaluation of
unloaded nonsubmerged and submerged implants
in the caninemandible. Journal of Periodontology
68: 1117–1130.
Hermann, J.S., Schofield, J.D., Schenk, R.K., Buser,
D. & Cochran, D.L. (2001) Influence of the size of
the microgap on crestal bone changes around titanium
implants. A histometric evaluation of unloaded
non-submerged implants in the canine
mandible. Journal of Periodontology 72: 1372–1383.
Jansen, V.K., Conrads, G. & Richter, E.J. (1997)
Microbial leakage and marginal fit of the implantabutment
interface. International Journal of Oral
& Maxillofacial Implants 12: 527–40.
Lazzara, R.J. & Porter, S.S. (2006) Platform switching:
a new concept in implant dentistry for controlling
postrestorative crestal bone levels.
International Journal Periodontics and Restorative
Dentistry 26: 9–17.
Ledermann, P.D., Schenk, R. & Buser, D. (1999)
Long-lasting osseointegration of immediately
loaded bar-connected TPS screws after 12 years
of function: a histologic case report of a 95-yearold
patient. International Journal Periodontics
and Restorative Dentistry 18: 553–556.
Linkow, L.I., Donath, K. & Lemons, J.E. (1992)
Retrieval analyses of a blade implant after 231
months of clinical function. Implant Dentistry 1:
37–43.
Misch, C.E., Bidez, M.W. & Sharawy, M. (2001) A
bioengineered implant for a predetermined bone
cellular response to loading forces. A literature
review and case reports. Journal of Periodontology
72: 1276–1281.
Morris, H.F., Ochi, S., Creum, P., Orenstein, I.H. &
Winkler, S. (2004) AICGR, Part I: a 6-year multicentered,
multidisciplinary clinical study of a new
and imnnovative implant design. Journal of Oral
Implantology 30: 125–133.
Nentwig, G.N. (2004) The Ankylos implant system:
concept and clinical application. Journal of
Oral Implantology 30: 171–177.
Neugebauer, J., Traini, T., Thams, U., Piattelli, A.
& Zoeller, J.E. (2006) Peri-implant bone organization
under immediate loading state: circularly
polarized light analyses. Journal of Periodontology
77: 152–160.
Papalexiou, V., Novaes, A.B., Grisi, M.F.M., Souza,
S.S.L.S., Taba, M. & Kajiwara, J.K. (2004) Influence
of implant microstructure on the dynamics
of bone healing around immediate implants placed
into periodontally infected sites. A confocal laser
scanning microscopic study. Clinical Oral Implants
Research 15: 44–53.
Persson, L.G., Lekholm, U., Leonhardt, A., Dahlen,
G. & Lindhe, J. (1996) Bacterial colonization on
internal surfaces of branemark system implant
components. Clinical Oral Implants Research
7: 90–95.
Piattelli, A., Corigliano, M., Scarano, A., Costigliola,
G. & Paolantonio, M. (1998) Immediate
loading of titanium plasma-sprayed implants: a
pilot study in monkeys. Journal of Periodontology
69: 321–327.
Piattelli, A., Corigliano, M., Scarano, A. & Quaranta,
M. (1997b) Bone reactions to early occlusal
loading of two-stage titanium plasma-sprayed implants:
a pilot study in monkeys. International
Journal Periodontics and Restorative Dentistry
17: 163–169.
Piattelli, A., Paolantonio, M., Corigliano, M. &
Scarano, A. (1997c) Immediate loading of titanium
plasma-sprayed screw-shaped implants in
man: a clinical and histological report of two
cases. Journal of Periodontology 68: 591–597.
Piattelli, A., Ruggeri, A., Trisi, P., Romasco, N. &
Franchi, M. (1993b) A histologic and histomorphometric
study of the bone reactions to non submerged
unloaded and loaded single implants in monkeys.
Journal of Oral Implantology 19: 314–320.
Piattelli, A., Scarano, A. & Paolantonio, M. (1997a)
Immediately loaded screw implant removed for
fracture after a 15-year loading period: histological
and histochemical analysis. Journal of Oral Implantology
23: 75–79.
Piattelli, A., Scarano, A., Paolantonio, M., Assenza,
B., Leghissa, G.C., Di Bonaventura, G., Catamo,
G. & Piccolomini, R. (2001) Fluids and microbial
penetration in the internal part of cement-retained
versus screw-retained implant–abutment connections.
Journal of Periodontology 72: 1146–1150.
Piattelli, A., Scarano, A. & Quaranta, M. (1997d)
High-precision, cost-effective system for producing
thin sections of oral tissues containing dental
implants. Biomaterials 18: 577–579.
Piattelli, A., Trisi, P., Romasco, N. & Emanuelli,
M. (1993a) Histological analysis of a screw implant
retrieved from man: influence of early loading
and primary stability. Journal of Oral
Implantology 19: 303–306.
Piattelli, A., Vrespa, G., Petrone, G., Iezzi, G.,
Annibali, S. & Scarano, A. (2003) Role of the
microgap between implant and abutment: a retrospective
histologic evaluation in monkeys. Journal
of Periodontology 74: 346–352.
Quirynen, M., Bollen, CM., Eyssen, H. & van
Steenberghe, D. (1994) Microbial penetration
along the implant components of the Branemark
system – An in vitro study. Clinical Oral
Implants Research 5: 239–44.
Quirynen, M. & van Steenberghe, D. (1993) Bacterial
colonization of the internal part of two-stage
implants. An in vivo study. Clinical Oral Implants
Research 4: 158–161.
Rocci, A., Martignoni, M., Burgos, P.M., Gottlow,
J. & Sennerby, L. (2003) Histology of retrieved
immediately and early loaded oxidized implants:
lightmicroscopic observations after 5 to 9 months
of loading in the posterior mandible. Clinical
Implant Dentistry& Related Research 5 (Suppl.):
88–98.
Romanos, G., Degidi, M., Testori, T. & Piattelli, A.
(2005) Histological and histomorphometrical
findings from human retrieved immediately functional
loaded implants. Journal of Periodontology
76: 1823–1832.
Romanos, G.E., Toh,C.G., Siar, C.H., Swaminathan,
D. & Ong, A.H. (2002) Histological and histomorphometric
evaluation of peri-implant bone subjected
to immediate loading: an experimental
study with Macaca Fascicularis. International Journal
of Oral & Maxillofacial Implants 17: 44–51.
Romanos, G., Toh, C.G., Siar, C.H., Swaminathan,
D., Ong, A.H., Donath, K., Yaacob, H. & Nent-
Degidi et al . Human immediately loaded implant
c
2007 The Authors. Journal compilation c 2007 Blackwell Munksgaard 281 | Clin. Oral Impl. Res. 19, 2008 / 276–282
wig, G.H. (2001) Peri-implant bone reactions to
immediately loaded implants. An experimental
study in monkeys. Journal of Periodontology 72:
506–511.
Rupp, F., Scheideler, L., Rehbein, D., Axmann, D.
& Geis-Gerstorfer, J. (2004) Roughness induced
dynamic changes of wettability of acid etched
titanium implant modification. Biomaterials 25:
1429–1438.
Siar, C.H., Toh, C.G., Romanos, G., Swaminathan,
D., ong, A.H., Yaacob, H. & Nentwig, GH. (2003)
Peri-implant soft tissue integration of immediately
loaded implants in the posterior macaque
mandible: a histomorphometric study. Journal of
Periodontology 74: 571–578.
Tarnow, D.P., Cho, S.C. & Wallace, S.S. (2000) The
effect of inter-implant distance on the height of
inter-implant bone crest. Journal of Periodontolology
71: 546–549.
Testori, T., Szmukler-Moncler, S., Francetti, L., Del
Fabbro, M., Scarano, A., Piattelli, A. & Weinstein,
R.L. (2001) Immediate loading of Osseotite
implants: a case report and histologic analysis
after 4 months of occlusal loading. International
Journal of Periodontics and Restorative Dentistry
21: 451–459.
Testori, T., Szmukler-Moncler, S., Francetti, L.,
Del Fabbro, M., Trisi, P. & Weinstein, R.L.
(2002) Healing of Osseotite implants under
submerged and immediate loading conditions
in a single patient: a case report and interface
analysis after 2 months. International Journal
Periodontics and Restorative Dentistry 22:
345–353.
Traini, T., Degidi, M., Caputi, S., Strocchi, R., Di
Iorio, D. & Piattelli, A. (2005a) Collagen fiber
orientation in human peri-implant bone of immediately
loaded titanium dental implants. Journal
of Periodontology 76: 83–89.
Traini, T., Degidi, M., Strocchi, R., Caputi, S. &
Piattelli, A. (2005b) Collagen fiber orientation
near dental implants in human bone: do their
organization reflect differences in loading? Journal
of Biomedical Materials Research Part B: Applied
Biomaterials 74B: 538–546.
Trisi, P., Emanuelli, M., Quaranta, M. & Piattelli,
A. (1993) A light microscopy, scanning electron
microscopy and laser scanning microscopy analysis
of retrieved blade implants after 7 to 20 years of
clinical function. Journal of Periodontology 64:
374–378.
Degidi et al . Human immediately loaded implant
282 | Clin. Oral Impl. Res. 19, 2008 / 276–282 c 2007 The Authors. Journal compilation c 2007 Blackwell Munksgaard