(105)2003 proussaefs, lozada the use of titanium mesh in conjunction with autogenous bone copia

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The International Journal of Periodontics & Restorative Dentistry

Since the acceptance of dental
implants as a valid treatment modal-
ity for the completely1,2 or partially3,4
edentulous patient, bone grafting
has been proposed before5–10 or
simultaneously6,10–12 with the place-
ment of dental implants to allow
their use in patients lacking ade-
quate bone volume. Several meth-
ods, materials, and techniques have
been used for bone grafting.
Extraoral6,11,12 and intraoral5–10,13
donor sites have been used when
autogenous bone grafting is
selected, while xenografts,14,15 allo-
plastic bone grafts,16,17 and allo-
grafts18,19 have also been proposed.
Various techniques have been
applied to secure the graft material
at the recipient site. Membranes,5,7
fixation screws,9,8,13 dental im-
plants,11,12 or titanium mesh20–29 are
the most common securing devices.
The current article provides a
clinical, radiographic, laboratory,
and histologic/histomorphometric
analysis of the use of titanium
mesh for localized alveolar ridge
augmentation in conjunction with
intraorally harvested intramem-
braneous autogenous bone graft
The Use of Titanium Mesh in
Conjunction with Autogenous Bone
Graft and Inorganic Bovine Bone
Mineral (Bio-Oss) for Localized Alveolar
Ridge Augmentation: A Human Study
Periklis Proussaefs, DDS, MS*
Jaime Lozada, DDS**
Alejandro Kleinman, DDS***
Michael D. Rohrer, DDS, MS****
Paul J. McMillan, PhD*****
This study evaluated the effects of using a titanium mesh for localized alveolar ridge
augmentation. Seven consecutively treated human subjects participated in the
study. Clinical, radiographic, laboratory, and histologic/histomorphometric analysis
revealed the efficacy of using the titanium mesh in conjunction with intraorally har-
vested autogenous bone graft and inorganic bovine bone mineral (Bio-Oss).
Radiographic measurements detected that a 2.86-mm vertical and 3.71-mm bucco-
labial ridge augmentation was achieved, while histomorphometry demonstrated
that 36.4% of the grafted area consisted of bone. Laboratory measurements
revealed 15.08% resorption of the graft for the first 6 months, which appeared to
consolidate after placement of the implants. Exposure of the mesh did not appear
to compromise the result. (Int J Periodontics Restorative Dent 2003;23:185–195.)
*****Assistant Professor, Graduate Program in Implant Dentistry, Loma
Linda University; and Private Practice, Prosthodontics and Implant
Dentistry, Santa Clarita, California.
*****Professor and Director, Graduate Program in Implant Dentistry,
Loma Linda University, California.
*****Assistant Professor, Graduate Program in Implant Dentistry, Loma
Linda University, California.
*****Professor and Director, Division of Oral and Maxillofacial Pathology,
University of Minnesota, Minneapolis.
*****Professor, Department of Pathology and Human Anatomy, School of
Medicine, Loma Linda University, California.
*****Reprint requests: Dr Periklis Proussaefs, Loma Linda University,
School of Dentistry, Graduate Program in Implant Dentistry, Loma
Linda, California 92350. e-mail: pproussaef@hotmail.com
185
Volume 23, Number 2, 2003

and inorganic bovine bone min-
eral.
Method and materials
Seven consecutively treated subjects
participated in this study (Table 1).
The subjects required a bone graft-
ing procedure before the placement
of dental implants. For all subjects,
a titanium mesh (Osteo-Tram,
Osteomed) was used during the
bone grafting procedure in con-
junction with an intraorally harvested
intramembraneous bone graft and
inorganic bovine bone mineral (Bio-
Oss, Osteohealth). The bone graft-
ing procedures were performed
from July 1998 to April 1999.
Treatment was performed at the
Center for Prosthodontics and
Implant Dentistry at Loma Linda
University (LLU). All subjects were
treated by residents of the graduate
program in implant dentistry and
signed the corresponding informed
consent form approved by the
Institutional Review Board at Loma
Linda University to have a biopsy
taken during implant surgery.
Surgical protocol
At the time of the bone grafting pro-
cedure or implant placement, the
subjects were given a choice of (1)
local anesthesia only, (2) local anes-
thesia with oral sedation (Halcion
0.25 mg, Upjohn), or (3) local anes-
thesia with intravenous sedation.
Full-thickness buccolabial and lin-
guopalatal flaps were reflected at
the recipient site (Fig 1). The donor
site was the chin area (three cases),
the ascending ramus area (three
cases), or an extraction socket (one
case) (Table 1). Harvesting of the
bone graft was performed according
to the standard procedure described
elsewhere.5,8 For the chin and
ascending ramus donor sites, the
autogenous bone graft was
removed in the form of a block (Fig
2) and then particulated with a
rongeur instrument (Blemental
Rongeur, H & H).
The autogenous graft particles
were mixed with inorganic bovine
bone mineral particles (Bio-Oss). The
recipient site was perforated to
induce bleeding and promote incor-
poration of the graft.30 The particu-
late graft was then placed at the
recipient site (Fig 3). A titanium mesh
(Osteo-Tram) was subsequently
trimmed to cover the recipient site
(Fig 4). Periosteal fenestration31,32
was performed along the bucco-
labial flap to enable primary closure.
The mesh was secured with fixation
screws (Fig 5). The flap was then
sutured.
Two weeks after the bone graft
surgery, the sutures were removed.
Six to 9 months were allowed for
the bone graft to heal before the
186
Table 1 Patient distribution
Age Recipient Healing No.of Type of provisional
Case (y) Sex site* Donor site (mo) implants restorations
1 60 M 12–23 Chin 9 5 Removable partial denture
2 70 M 13–12 Ramus 6 2 Fixed partial denture
3 67 F 13–23 Ramus 6 6 None
4 54 F 46–47 Ramus 8 2 None
5 69 M 17–16 Chin 6 2 None
6 44 M 11–22 Chin 6 3 None
7 77 F 17–15 Extraction site 13 3 None
Mean 63 7.71
SD 11.16 2.62
Range 44–77 6–13
*Fédération Dentaire Internationale tooth-numbering system.
SD = standard deviation.

placement of the implants (Fig 6
and Table 1). One subject (case 7)
received the implants 13 months
after the bone grafting procedure
because she was unable to return
earlier for personal reasons. The
titanium mesh was removed 1 to 2
months before the placement of the
implants in a separate procedure.
Full-thickness buccolabial and lin-
guopalatal flaps were reflected, and
the mesh was removed after
unscrewing the fixation screws (Fig
7). Hydroxyapatite-coated root-form
implants (Steri-Oss, Nobel Biocare)
placement of the implants (after the
bone grafting had healed). For three
subjects, a computed tomographic
(CT) scan was taken before the bone
grafting procedure and before
placement of the implants (Figs 11
and 12), whereas for the other four
subjects, linear tomographs were
taken at the same intervals.
Measurements for the vertical
and buccolabial bone augmentation
were made by evaluating the pre-
operative and postoperative peri-
apical radiographs in conjunction
with the linear tomographs or CT
were placed 1 to 2 months after the
removal of the mesh with the aid of
a surgical stent (Fig 8). All cases were
treatment planned to receive an
implant-supported screw-retained
fixed partial denture (Figs 9 and 10).
Radiographic evaluation
All subjects received preoperative
and postoperative panoramic radi-
ographs. In addition, periapical radi-
ographs were taken before the bone
grafting procedure and before the
187
Fig 1 Full-thickness labiopalatal flaps are
reflected to expose the residual alveolar
ridge.
Fig 2 Autogenous bone graft is harvest-
ed from the chin area.
Fig 3 Autogenous bone graft is mixed
with inorganic bovine bone mineral (Bio-
Oss) and placed at the recipient site.
Fig 4 Titanium mesh is trimmed and
placed over the graft material.
Fig 5 Titanium mesh is secured in place
by three fixation screws.
Fig 6 Healing of the grafted area
6 months after the bone augmentation
procedure. No mesh exposure or mucosa
irritation is noted.

scans. All measurements were made
by one investigator. For the linear
tomographs, the distortion rate (1.7)
provided by the manufacturer of the
tomographic unit (Scanora type SBR
1C, Orion) was taken into consider-
ation when the measurements were
made. All tomographs were taken
under the same series of linear pro-
jection (numbers provided by the
manufacturer). The position of the
subject’s head was standardized by
two light lines (one vertical and one
horizontal) that are incorporated into
the unit so the intersection of the
two lines was located at the midline
between the eyes of the subject
(horizontal level reference) and at
the midline between the eyebrows
(vertical level reference).
Laboratory evaluation
Irreversible hydrocolloid impressions
(Coe Alginate, GC) were made
around the grafted area with a cus-
tom tray made from photopolymer-
ized acrylic resin (Triad, Dentsply).
The impressions were made preop-
eratively, 1 month after the bone
grafting procedure, 6 months after
bone grafting, and 6 months after
implant surgery. The impressions
were poured with type III dental
stone (Microstone, Whip-Mix). The
postoperative stone casts were used
to quantitatively assess the volume
of the alveolar ridge augmentation
by adhering to a technique devel-
oped at LLU.33,34 Briefly, a custom
tray was fabricated from photopoly-
merized acrylic resin. An impression
was made from the postoperative
stone cast using the custom tray and
silicone impression material (Lab-
putty, Coltene/Whaledent). Polyvinyl
siloxane bite registration material
(Exabite II NDS, GC) was loaded in
the tray, which was then placed on
the preoperative stone cast, and the
188
Fig 7 Recipient site after the mesh is
removed.
Fig 8 One month after mesh removal,
dental implants are placed with the aid of
a surgical stent.
Fig 9 Final result, facial view.
Fig 10 Patient’s smile with the definitive
prosthesis.
Fig 11 CT scan, preoperative view. Fig 12 CT scan, postoperative view.

registration material was allowed to
polymerize (Fig 13). The weight of
the registration material was asses-
sed, and by considering the weight
provided by the manufacturer, it was
possible to calculate the volume of
the alveolar ridge augmentation. In
addition, linear measurements were
made with a caliper (Darby Dental
Supply) by evaluating the bucco-
labial thickness and vertical height of
the registration material.
During implant surgery, a biopsy
was taken from the grafted area
using a 2-mm-internal-diameter
trephine bur (ACE Surgical Supply)
as the first drill during the osteotomy
preparation for implant placement.
The specimens were fixed in 10%
buffered formalin. The specimens
were dehydrated in alcohol and
embedded in specialized resin
(Technovit 7200 VLC, Heraeus
model BH-2, McBain Instruments).
For each specimen, one to three
images were analyzed, depending
on the size of the specimen.
Results
Clinical evaluation
Exposure of the mesh during healing
was observed in four of the seven
cases (Table 2). In these cases, soft
tissue proliferation and epithelializa-
tion was noticed to occur under-
neath the exposed mesh, an obser-
vation also made by others.24 Oral
hygiene instructions included to
gently brush the exposed mesh with
a T-ended toothbrush. Patients re-
ported no pain or discomfort at the
grafted area, even when the mesh
was exposed. No clinical sign of
Kulzer). Initial midaxial sections of
200 µm were made by means of the
cutting-grinding system (Exakt
Medical Instruments). The sections
were then ground to 40 to 50 µm
and stained with Stevenel’s blue and
van Gieson’s picric fuchsin for histo-
morphometric analysis and light
microscopy.35,36
Histomorphometric evaluation
was performed by one investigator
using a computer-assisted linear
analysis program, Ribbon, devel-
oped at LLU.37 For each specimen,
the following parameters were mea-
sured: percentage composition of
bone, connective tissue, and residual
Bio-Oss, and percentage of the sur-
face of the Bio-Oss surface in direct
contact with bone. All histomorpho-
metric analysis was performed by
capturing an image under 2ϫ mag-
nification (Olympus Microscope,
189
Fig 13 Laboratory measurements allow
linear and volumetric measurements of the
grafted area. The blue area (bite registra-
tion material) represents the augmented
alveolar ridge. The white area represents
the custom tray. An impression with sili-
cone (pink) is made from the postoperative
stone casts, bite registration material is
internally applied, and the tray is reseated
on the preoperative (before the bone aug-
mentation) stone cast.
Table 2 Clinical assessment*
Bone Complications, Complications,
Case quality donor site recipient site
1 II Prolonged hypesthesia, None
finally resolved
2 III None Mesh exposure,4 mm ϫ 5 mm
3 II None None
4 III None Mesh exposure,3 mm ϫ 7 mm
5 IV None Mesh exposure,4 mm ϫ 5 mm
6 III Incision line dehisced Mesh exposure,4 mm ϫ 7 mm
7 IV None None
*In all cases,the Bio-Oss particles appeared well-attached to the surrounding grafted area and incor-
porated into the regenerated alveolar ridge.

inflammation or infection was
observed in any of the seven cases.
During the removal of the mesh,
a layer of connective tissue was con-
sistently observed underneath the
mesh. Boyne et al21 described this
layer as “pseudoperiosteum.” The
mesh was surrounded by a thin layer
of granulation tissue in most cases.
The Bio-Oss particles appeared well-
incorporated into the grafted area.
During implant placement, the
grafted area had a type II to IV con-
sistency. Primary stability was
achieved during the placement of
all implants.
Radiographic evaluation
Radiographic analysis revealed that
a 2.86-mm vertical ridge augmenta-
tion (range 1 to 5 mm, standard devi-
ation [SD] 1.77) and a 3.71-mm buc-
colabial augmentation (range 2 to 5
mm, SD 1.24) were achieved. In all
cases, adequate bone volume was
clinically observed for the placement
of root-form implants in a prosthet-
ically ideal position.
Laboratory evaluation
Laboratory volumetric measure-
ments revealed that 1.26 mL of ridge
augmentation was achieved 1
month postoperative, 1.07 mL was
achieved 6 months after bone graft-
ing, and 1.05 mL was achieved 6
months after implant placement
(Table 3). These measurements dic-
tated a 15.08% resorption 6 months
after bone grafting, which appeared
to consolidate after the placement of
the implants. Linear measurements
revealed that 1 month after the bone
grafting procedure, 3.14 mm of ver-
tical and 4.28 mm of buccolabial
ridge augmentation were obtained
(Table 4). The corresponding num-
bers for the 6-month postgrafting
measurements were 2.57 mm of ver-
tical and 3.86 mm of buccolabial
alveolar ridge augmentation, while 6
months after implant placement, the
corresponding numbers were 2.71
mm and 3.71 mm, respectively.
In all specimens, a mixture of
bone, connective tissue, and resid-
ual Bio-Oss particles was observed
(Fig 14). In the majority of the cases,
the Bio-Oss particles appeared to
be in tight contact with bone (Figs 15
and 16). No signs of resorption or
active inflammatory processes were
identified in any of the specimens.
The mean area of all seven core
sections occupied by bone was
36.4% (Table 5). The comparable
value for soft tissue was 51.6%, and
for Bio-Oss particles it was 12.0%.
The proportion of the surface of
residual Bio-Oss particles that was in
contact with bone was 36.7%.
Discussion
The current study provided histo-
logic evidence in humans that the
use of titanium mesh in conjunction
with autogenous bone graft and
inorganic bovine bone mineral (Bio-
Oss) can result in new bone forma-
tion. In the literature, there is a
scarcity of histologic evidence in
humans of the results obtained using
a titanium mesh for alveolar ridge
augmentation. Although animal
studies have offered the opportu-
nity to histologically evaluate the
results of this method of bone graft-
ing,20,23 few papers have reported
histologic evidence of bone forma-
tion in humans after alveolar ridge
190
Table 3 Volume of alveolar ridge augmentation (mL)
1 mo after 6 mo after 6 mo after implant
Case grafting grafting placement
1 0.87 0.73 0.69
2 0.45 0.33 0.30
3 3.05 2.73 2.82
4 1.25 1.00 0.95
5 1.03 0.87 0.81
6 0.47 0.33 0.34
7 1.72 1.50 1.44
Mean 1.26 1.07 1.05
SD 0.99 0.90 0.87
Range 0.45–3.05 0.33–2.73 0.30–2.82

191
Table 4 Linear laboratory measurements (mm)
1 mo after grafting 6 mo after grafting 6 mo after implant placement
Case Vertical Buccolabial Vertical Buccolabial Vertical Buccolabial
1 2 5 1 4 1 4
2 3 4 3 4 3 4
3 2 6 2 6 2 6
4 4 3 3 2 3 2
5 4 2 3 2 4 2
6 3 4 2 4 2 3
7 4 6 4 5 4 5
Mean 3.14 4.28 2.57 3.86 2.71 3.71
SD 0.90 1.50 0.97 1.46 1.11 1.50
Range 2–4 2–6 1–4 2–6 1–4 2–6
Fig 14 Histologic overview (Stevenel’s
blue–van Gieson’s picric fuchsin stain; orig-
inal magnification ϫ 3).
Fig 15 Residual bovine bone mineral
(Bio-Oss) particles are in tight contact with
the surrounding bone. Particles appear
interconnected with bony tissue. No sign
of inflammation or resorption is observed
(Stevenel’s blue–van Gieson’s picric fuchsin
stain; original magnification ϫ 10).
Fig 16 At higher magnification, some of
the residual Bio-Oss particles appear to
have an intimate contact with the sur-
rounding bone along the entire surface
(Stevenel’s blue–van Gieson’s picric fuchsin
stain; original magnification ϫ 20).
Table 5 Histomorphometric analysis (%)
Fibrous Residual Bio- Bone–residual
Case Bone tissue Oss particles particles contact
1 40 52 8 22
2 24 62 14 0
3 36 54 10 35
4 34 53 13 45
5 30 57 13 63
6 53 45 2 50
7 38 38 24 42
Mean 36.4 51.6 12.0 36.7
SD 9.05 7.89 6.71 20.54
Range 24–53 38–62 2–24 0–63

augmentation using a titanium
mesh.25,26,28,29
Regarding the type of bone
grafting that has been used in con-
junction with a titanium mesh, the
majority of the reported cases
involved the use of extraorally har-
vested autogenous endochondral
bone grafts, typically from the iliac
crest area.20–23,25,28 However,
hydroxyapatite25 or Bio-Oss29 mixed
with autogenous bone has also been
proposed, as has the use of intra-
membraneous autogenous bone
grafts harvested intraorally from
the chin or ascending ramus
area.24,26,27,29 Several publications
have demonstrated a superiority of
the intramembraneous autogenous
bone graft to the extraorally har-
vested endochondral graft.38–42
Intraorally harvested grafts have
demonstrated a reduced resorption
rate,38,39,41 faster rate of revascular-
ization,40,41 and accelerated healing
process42 attributed to their embryo-
genic origin. A 15.08% resorption of
the graft was observed in the current
study 6 months after the bone aug-
mentation procedure according to
the measurements performed in the
laboratory. The volume of the
grafted area appeared to consoli-
date after placement of the implants,
an observation also made by oth-
ers.43 The occlusal or transmucosal
loads of the implants may provide
stimulus to the periimplant bone to
maintain the bone volume.44
During harvesting of the auto-
genous bone graft, an effort was
made to harvest bone marrow in the
largest possible quantity. The chin
area appears to offer an increased
amount of bone marrow compared
to other intraoral donor sites.8 Can-
cellous bone marrow offers en-
hanced bone formation at the recip-
ient site.45,46 Revascularization of
cancellous bone is faster, and en-
dosteal osteoblasts and marrow
mesenchymal cells that are capable
of bone induction are transplanted.
In addition, the autogenous bone
grafts in the current study were par-
ticulated, since particulate bone
grafts have been associated with
enhanced healing and revascular-
ization processes.46
Inorganic bovine bone mineral
(Bio-Oss) was used as a filler in the
current study. This material appeared
to be biocompatible and histologi-
cally demonstrated tight contact
with the surrounding bone at 36.7%
of its surface area. In one case (case
2), the Bio-Oss particles had no con-
tact with the surrounding bone. In
that case, the fixed temporary pros-
thesis had fractured, impinging on
the grafted area during function. It
can be hypothesized that the micro-
movement induced on the Bio-Oss
particles in that case prevented bone
formation in tight contact with the
particles. No sign of resorption or
inflammation was observed under
light microscopy.
The effectiveness and biocom-
patibility of Bio-Oss when used as an
inlay bone graft has been well-doc-
umented in both animal47,48 and
human studies.49,50 However, little is
known about the use of Bio-Oss as
an onlay bone graft. In a four-walled
defect in rabbits, the use of Bio-Oss
resulted in the formation of new
bone between the particles of the
graft that were in tight contact with
the surrounding bone, with no sign
of resorption or inflammation.51
Similar observations have been
made in humans.15,29,52 On the other
hand, some studies14,53 failed to
identify any bone formation around
Bio-Oss particles when used as an
onlay bone graft. However, when
Bio-Oss is mixed with an autoge-
nous bone graft, as in the current
study, new bone formation is
observed. The inorganic bovine
bone mineral acts as a scaffold for
the formation of new bone. It
appears that there is a need for an
autogenous bone graft with the
osteogenic potential to induce new
bone formation around the Bio-Oss
particles.29,52 Further studies are
needed to assess the role of this
xenograft when used as an onlay
bone graft.
Exposure of the titanium mesh
was observed in four of the cases in
the current study. This is a common
phenomenon when a titanium mesh
is used for alveolar ridge augmen-
tation, and von Arx et al24 experi-
enced exposure of the mesh in 50%
of their cases. However, clinically
and histologically, the exposure did
not appear to affect the final out-
come. This offers an advantage
compared to nonresorbable mem-
brane barriers, which result in infec-
tion when exposed.7 In the current
study, the titanium mesh was
removed 1 to 2 months before the
placement of the implants as a sep-
arate procedure. The presence of a
thin layer of granulation tissue
around the mesh dictated the
removal in a separate approach.
192

Multiple surgical procedures (bone
grafting, titanium mesh removal,
implant placement, implant uncov-
ering) increase the time, cost, and
discomfort associated with the treat-
ment.
The laboratory technique used
in the current study to provide volu-
metric and linear measurements of
the alveolar ridge augmentation has
been shown to be both reproducible
and accurate.33,34 However, for the
current study, the impressions were
made from the residual alveolar
ridge before and after the bone
grafting procedure. The major limi-
tation is that this does not include
measurements of the soft tissue
thickness. Alternatively, the impres-
sions could be made directly from
the bone and during the surgery,
excluding the variability induced by
the soft tissue thickness.
The present study demon-
strated 36.4% bone formation when
titanium mesh was used in conjunc-
tion with an autogenous bone graft
and Bio-Oss. The augmented alve-
olar ridges had a solid consistency,
and no sign of inflammation or
resorption was seen under light
microscopy. The grafted areas
demonstrated a 15.08% resorption
in the 6 months after bone grafting,
which appeared to consolidate after
implant placement. Radiographic
assessment revealed a 2.86-mm ver-
tical and 3.71-mm buccolabial ridge
augmentation, and exposure of the
mesh did not appear to compromise
the result.
Acknowledgments
The authors would like to acknowledge
Osteomed and Nobel Biocare for support-
ing the study and ACE Surgical Supply for
providing the trephine burs. They would like
also to thank Andre Torres, DDS, MSD, for his
contribution. They are also thankful to Hari
Prasad, BS, MDT, for his technical assistance
during the histologic processing. The first
author is much obliged to Dimitris Tatakis,
DDS, PhD, for his overall guidance and con-
tribution, and to Gloria Valencia, DDS, for her
priceless support.
193

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