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One-stage horizontal guided bone regeneration with autologous bone,

anorganic bovine bone and collagen membranes: Follow-up of a prospective
study 30 months after loading

Article  in  European Journal of Oral Implantology · October 2018

DOI: 10.1111/clr.291_13358

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 ORIGINAL ARTICLE „ 89

Silvio Mario Meloni, Sascha Alexander Jovanovic, Milena Pisano, Giacomo De Riu, Edoardo Baldoni,
Marco Tallarico

One-stage horizontal guided bone regeneration

with autologous bone, anorganic bovine bone and
collagen membranes: Follow-up of a prospective
study 30 months after loading Silvio Mario Meloni,
DDS, MSc, PhD
Adjunct Professor at the
School Periodontology of
Dentistry, University of
Sassari, Italy. Specialist in
Key words autogenous bone, bone substitute, dental implants, guided bone regeneration Oral Surgery, EAO Certified
in Implant-based Therapy

Purpose: To present the medium-term results of one-stage guided bone regeneration (GBR) using Sascha Alexander
autologous bone and anorganic bovine bone, placed in layers, in association with resorbable collagen Jovanovic, DDS, MSc
Assistant Professor, Implant
membranes, for the reconstruction of horizontal bony defects. Program, Loma Linda Univer-
sity; Private Practice in Los
Materials and methods: This study was designed as an uncontrolled prospective study. Partially Angeles, USA
edentulous patients, having less than 6.0 mm and more than 4.0 mm of residual horizontal bone
Milena Pisano, DDS
width were selected and consecutively treated with simultaneously implant installation and bone Private Practice, Arzachena,
regeneration by using 2.0 mm of autologous bone and 2.0 mm of anorganic bovine bone that was Italy

placed in layers and then covered with a resorbable collagen membrane. Outcome measures were: Giacomo De Riu, MD,
implant and prosthesis failures, any complications, peri-implant marginal bone level changes, probing MS
Assistant Professor, University
pocket depth (PPD) and bleeding on probing (BOP). of Sassari, Italy
Results: In total, 45 consecutive patients (20 male, 25 female) with a mean age of 52.1 years Edoardo Baldoni
each received at least one GBR procedure, with contemporary placement of 63 implants. At Professor, School of Dentistry
University of Sassari, Italy.
the 3-year follow-up examination, no patient had dropped out and no deviation from the ori-
ginal protocol had occurred. No implant or prosthesis failed. In six patients (13.3%) the collagen Marco Tallarico, DDS,
MSc
membrane was slightly exposed 1 to 2 weeks after bone reconstruction. Four of these patients Adjunct Professor, Aldent
were moderate smokers. Post-hoc analysis using Fisher’s exact test found significant association University, Tirana, Albania;
Private Practice, Rome, Italy
(P = 0.0139) between a smoking habit and early membrane exposure. Mean marginal bone
loss experienced between initial loading and 30 months afterwards was 0.60 ± 0.20 mm (95% Correspondence to:
Silvio Mario Meloni
CI 0.54 – 0.66). The mean BOP values measured at the definitive restoration delivery were Via Ippolito Nievo SNC,
07021 Arzachena,
1.23 ± 0.93, while 2 years later they were 1.17 ± 0.78. The difference was not statistically sig- Email: melonisilviomario@
nificant (-0.06 ± 0.76; P = 0.569). The mean PPD values measured at the definitive restoration yahoo.it

delivery were 2.62 ± 0.59 mm, while 2 years later they were 2.60 ± 0.54 mm. The difference was
not statistically significant (-0.03 ± 0.62; P = 0.765).
Conclusions: Within the limitations of the present study, the use of a 2.0 mm layer of particulated
autologous bone on the implant threads, and a 2.0 mm layer of anorganic bovine to cover the
resorbed ridge, in combination with the resorbable collagen membrane, seems to be a viable treat-
ment option for the reconstruction of horizontal bony defects.

Conflict of interest statement: This study was not supported by any company, and there are no
conflicts of interest.

Eur J Oral Implantol 2018;11(1):89–95

90 „ Meloni et al Horizontal guided bone regeneration
„ Introduction
Prosthetic rehabilitations on osseointegrated den-
tal implants are a valid treatment option to restore
edentulous ridges. However, several factors can be
involved in the success of implant therapy. Of these,
bone volume at implant insertion represents one of
the most important factors for predictable long-term
results1. Indeed, unfavourable local conditions, such
as insufficient bone volumes, can negatively affect the
prognosis of dental implants2,3. In 1988, Cawood and
Howell classified the atrophy degree of edentulous
jaws into six classes4. Atrophies of class III present a
medium horizontal defect, complicating the correct
placement of regular implants without exposure of
threads. Many techniques have been developed to
reconstruct atrophic alveolar jaws for the placement
of dental implants, either in combination with graft
procedures or in a two-stage surgery after a period
of healing5. GBR for horizontal augmentation has
been described in numerous studies showing repro-
ducible results and high, long-term implant survival
rates6,7. Similar implant survival rate was achieved
when GBR was combined with either simultaneous
or subsequent implant placement, indicating that the
two approaches may be comparable7. Similar implant
survival rates may also be achieved when the implant
is placed in augmented or native bone8. Nevertheless,
according to recent literature reports9,10, in the case of
severe horizontal ridge atrophy and vertical defects, a
two-stage approach seems to be a safer procedure9.
When is possible to reach a sufficient primary implant
stability, bone augmentation procedures could be per-
formed in a one-stage approach11.
Resorbable membranes, in combination with
particulated anorganic bovine bone, can be used for
the augmentation of horizontally deficient ridges12.
Particulated autogenous bone can be mixed with
bone substitutes to add more osteogenic factors9,13.
The aim of this prospective cohort study is to
present the medium-term results of the one-stage
approach using autologous bone and anorganic
bovine bone placed in layers, in association with
resorbable collagen membranes, for the augmenta-
tion of horizontal bone defects. This report was writ-
ten in accordance with the STROBE (STrengthening
the Reporting of OBservational studies in Epidemiol-
ogy) guidelines (http://www.strobe-statement.org).
Eur J Oral Implantol 2018;11(1):89–95
„ Materials and methods
All patients were informed about the nature of the
treatment and their written consent was obtained.
Data collection was designed to preserve patient ano-
nymity. The present prospective study evaluated data
collected from any partially edentulous patient, aged
18 years or older, rehabilitated with anodised sur-
face implants (TiUnite, Nobel Biocare AB, Göteborg,
Sweden) placed in the alveolar crest with 4.0 mm to
6.0 mm width between January 2012 and December
2012. One clinician (SMM), who has expertise in den-
tal implant placement and guided bone regeneration,
performed all the surgical procedures and another
(MP), who is experienced in implant-supported pros-
thesis, performed all prosthetic procedures in one pri-
vate practice centre in Arzachena, Sardinia, Italy.
Inclusion criteria were: patients aged 18 years
or older, who presented with partial edentulism of
the mandible or maxilla, with a residual horizontal
ridge of more than 4.0 mm and less than 6.0 mm,
who required an implant supported restoration, and
able to understand and sign an informed consent.
Patients were not admitted on to the study if any of
the following exclusion criteria was present:
1. American Society of Anaesthesiologists (ASA)
class III or IV;
2. Psychiatric contraindications;
3. Pregnancy or nursing;
4. Alcohol or drug abuse;
5. Heavy smoking (> 10 cigarettes/day);
6. Radiation therapy to head or neck region within
5 years;
7. High and moderate parafunctional activity;
8. Absence of teeth/denture in the opposite jaw;
9. Untreated periodontitis;
10. Immediate post-extractive implants;
11. Full mouth bleeding and full mouth plaque index
of 25% or higher;
12. Unable to attend regular follow-ups.
„ Surgical and prosthetic protocol
The patients’ medical history was collected and study
models were made. Preoperative photographs and
radiographs, including cone beam computer tomog-
raphy (CBCT) or CT scans, were obtained for initial
screening and evaluation (Fig 1). After diagnostic

Fig 1 Pre-operative picture.
Fig 3 2.0 mm layer of autologous Fig 4 2.0 mm layer of anorganic
bone. bovine bone.
wax-up of the ideal prosthetic and aesthetic position
of the teeth, implant positions were planned with the
ideal soft tissue contour and prosthetic position. After
careful functional and aesthetic evaluation, a sur-
gical template was fabricated. Patients received 2 g
of amoxicillin (Zimox, Pfizer, Rome, Italy) 1 h before
surgery and then 1 g twice daily for 1 week. Patients
allergic to penicillin received 600 mg of clindamycin
1 h before surgery, then a 300 mg dose four times a
day for 1 week. Patients rinsed with 0.2% chlorhexi-
dine solution (Curasept, Curaden Healthcare, Saronno,
Varese, Italy) for 1 min to disinfect the surgical site and
a sterile surgical drape was applied to minimise the
potential contamination from extraoral sources. Local
anaesthetic (Septanest with adrenaline, 1/100,000,
Septodont, Saint-Maur-des-Fossés, France) was used.
A mid-crestal incision into the keratinised tissue
was made using a surgical blade, and the full-thick-
ness flaps were elevated beyond the mucogingival
junction and at least 5.0 mm beyond the bone defect.
Meloni et al Horizontal guided bone regeneration „ 91
Fig 2 Implant placement in atrophic
ridge.
Fig 5 Collagen membrane fixed with
titanium pins to cover the bone graft.
Two vertical incisions were made at least one tooth
away from the area to be augmented. In the posterior
mandible, a lingual flap was elevated, and maxilla and
mandible-sensitive anatomic structures (e.g. mental
and infraorbital nerves) were protected. Before bone
harvesting, the recipient site was cleared of all soft
tissue remnants. Autogenous bone was harvested
using a minimally invasive cortical bone collector
(Safe Scraper, Micross, Meta, Reggio Emilia, Italy).
Multiple decortication holes at the recipient site were
performed with a 2.0 mm round bur. Implants were
inserted guided by a pre-fabricated surgical template.
Exposed threads were first covered with a layer of
2.0 mm of autologous bone (Figs 2 and 3) positioned
on the titanium surface, while a second layer of
anorganic bovine bone material (Bio-OSS, Geistlich
Biomaterials Italia, Thiene, Vicenza, Italy) was pos-
itioned on top and to cover the autogenous bone
over a 2.0 mm width (Fig 4). A resorbable collagen
membrane (Bio-gide, Geistlich Biomaterials) (Fig 5)
Eur J Oral Implantol 2018;11(1):89–95
92 „ Meloni et al Horizontal guided bone regeneration
Fig 6 Prosthesis, 2 years after delivery of the definitive
prosthesis.
was fixed with titanium pins (Supertack, MCbio,
Lomazzo, Como, Italy) on the lingual/palatal side.
The membrane was trimmed to cover the entire
volume of the graft and additional titanium pins
were positioned on the vestibular side. A periosteal
incision between the two vertical incisions was per-
formed to allow the flap to be closed completely,
tension-free. In the mandible, both the lingual and
the buccal flaps were released. The flaps were then
sutured in two layers to prevent exposure of the
membrane. Horizontal mattress sutures (4-0 Vycril,
Ethicon, Johnson & Johnson, Pomezia, Italy) were
first placed 4.0 mm from the incision line before
single interrupted sutures were placed near the
edges of the flaps (4-0 Vycril). Vertical incisions
were sutured with single, interrupted sutures. These
were then removed after between 10 and 14 days
post-surgery, while mattress sutures were removed
2 to 3 weeks after surgery.
Postoperatively, 80 mg of ketoprofen (Oki,
Dompé, Milan, Italy) were prescribed twice or three
times a day, as needed. A 4 mg/day dose of dexa-
methasone (Desoren, Rekah Pharmaceutical Prod-
ucts, Holon, Israel) was administered for an addi-
tional 2 days. Patients were instructed to rinse with
0.2% chlorhexidine (Curasept) for 2 weeks and to
follow a soft food diet for 10 days.
Six months after implant placement, temporary
crowns were delivered and 6 months later Com-
puter-aided design/computer-assisted manufac-
ture (CAD/CAM), screw-retained, zirconia ceramic
crowns were delivered. All patients were followed
up to 3 years after implant placement (Figs 6 and 7).
Eur J Oral Implantol 2018;11(1):89–95
Fig 7 Peri-apical radiograph
2 years after delivery of the
definitive prosthesis.
Patients were monitored to evaluate the following
parameters: absence of pain, foreign-body sensa-
tion and/or dysesthesia, and radiologic contact
between the host bone and the implant surface.
„ Outcome measures
Primary outcome measures
Implant/crown failure:
Removal of implants dictated by implant mobility,
progressive marginal bone loss, infection, or im-
plant fracture. The stability of individual implants
was measured by the prosthodontist at the time
of temporary and definitive crown delivery (6 and
12 months after implant placement, respectively) by
applying 35 Ncm of removal torque. After 24 and
then 36 months following implant placement, im-
plant stability was tested manually by the same pros-
thodontist using two dental mirror handles.
Complications:
Any complications, such as membrane exposure,
subsequent infection, and/or morbidity associated
with the harvest site, any prosthetic complications,
such as fractures or chipping of the provisional or
definitive ceramic crown, abutment mobility and any
biological complications, such as wound or implant
infection, mucositis, abscesses, or peri-implantitis,
were recorded.

„ Secondary outcome measures
Peri-implant marginal bone loss:
The distance from the most coronal margin of the im-
plant collar and the most coronal point of bone-to-
implant contact, evaluated on intraoral digital radio-
graphs taken with the paralleling technique using a
film-holder (Rinn XCP, Dentsply, Elgin, IL, USA) at
implant placement, initial loading (after 6 months),
definitive restoration delivery (after 1 year), and after
2 years. The radiographs were accepted or rejected
for evaluation based on the clarity of the implant
threads. All readable radiographs were displayed in
an image analysis programme (DFW2.8 for Win-
dows, Soredex) on a 24-inch LCD screen (iMac,
Apple, Cupertino, CA, USA). The software was cali-
brated for every single image using the known dis-
tance of two adjacent threads. Measurements of the
mesial and distal bone crest level adjacent to each
implant were made by a clinician (AD) to the nearest
0.01 mm and averaged at patient level.
Soft tissue parameters:
Probing pocket depth (PPD) and bleeding on probing
(BOP) were measured by an operator (AD), who had
not previously been involved in the present study,
using a periodontal probe (PCP-UNC 15, Hu-Friedy
Manufacturing, Chicago, IL, USA) at definitive res-
toration delivery and then 2 years later (36 months
after implant placement). Three vestibular and three
lingual measurements were collected for each im-
plant, and averaged at patient level.
„ Statistical analyses
Data analysis was carried out according to a pre-
established analysis plan. Post-hoc analysis was per-
formed to detect any possible association between
smoking and the risk of membrane exposure. Patient
data were compiled from the records of the eli-
gible patients using an Excel spreadsheet (Micro-
soft) that reflected the parameters in the patient
records. A clinician (MT) with expertise in dentistry
analysed the data using SPSS for Windows release
18.0 (SPSS, Chicago, IL, USA). Descriptive ana-
lysis was performed for numeric parameters using
Meloni et al Horizontal guided bone regeneration „ 93
means ± standard deviations (95% confidence inter-
val, CI). Comparisons between each time point and
the baseline measurements were made by paired
tests, to detect any changes in volumetric dimen-
sional of the ridge. The differences in the proportion
of patients with complications were analysed using
Fisher’s exact test. The patient was the statistical
unit of the analyses. Median and inter-quartile range
(IQR) values were also calculated for BoP and PPD
in order to give a better description of the data set.
All statistical comparisons were conducted at the
0.05 level of significance.
„ Results
Fifty patients were screened for eligibility, but five
patients were not enrolled because of their refusal to
sign the research informed consent. Forty-five con-
secutive patients (20 males 25 females; mean age
of 52.1 years, range 24 to 78), with 63 implant sites
classified as Cawood-Howell Class III4, each received
at least one GBR procedure, with contemporary
placement of 63 implants (NobelReplace Conical
Connection, PMC, Nobel Biocare). Thirteen out of
the 45 patients (28.8%) were moderate smokers.
At the 3-year follow-up examination, no patient
had dropped out and no deviation from the original
protocol had occurred. All the collected data were
included in the statistical analysis. No implant failed
and no prosthetic complication was observed. No
major biological complications were recorded. In
six patients (13.3%) the collagen membrane was
slightly exposed 1 to 2 weeks after bone augmenta-
tion. Four of these patients were moderate smokers.
Post-hoc analysis using Fisher’s exact test found a
significant association (P = 0.0139) between smok-
ing and early membrane exposure. Patients with
exposure were treated with local application of
chlorhexidine gel 0.5% (Curasept ADS 0.5% gel
parodontale, Curaden Healthcare) twice a day for
3 weeks in the exposed area. Complete soft tissue
healing was observed in all cases.
Mean marginal bone level at implant placement
was 0.12 ± 0.14 mm (95% CI 0.11 – 0.19). At the
initial loading (6 months after implant placement),
mean marginal bone level was 0.17 ± 0.10 mm (95%
CI 0.17 – 0.23). The difference was 0.05 ± 0.09 mm
Eur J Oral Implantol 2018;11(1):89–95
94 „ Meloni et al Horizontal guided bone regeneration

Table 1 Marginal bone levels and loss within follow-ups [mm ± SD (95% CI)].

Implant placement Initial loading Definitive loading 30 months after initial

loading
Marginal bone N = 45 N = 45 N = 45 N = 45
levels 0.12 ± 0.14 0.17 ± 0.10 0.61 ± 0.21 0.77±0.22
(0.11 – 0.19) (0.17 – 0.23) (0.54 – 0.66) (0.70 – 0.82)
Initial loading – 30 months after initial 30 months after initial 30 months after initial
Implant placement loading – Initial loading – Definitive loading – Implant
loading loading placement
Marginal bone N = 45 N = 45 N = 45 N = 45
loss 0.05 ± 0.09 0.60 ± 0.20 0.16 ± 0.08 0.65 ± 0.18
(0.01 – 0.07) (0.54 – 0.66) (0.16 – 0.20) (0.60 – 0.69)
P value 0.0004 0.0000 0.0000 0.0000

Table 2 PPD and BOP within follow-up.

Implant placement Definitive restoration delivery 2 years later

BoP NA N = 45 N = 45
1.23 ± 0.93 1.17 ± 0.78
(IQR 0.75; 1.00; 2.00) (IQR 1.00; 1.00; 2.00)
PPD NA N = 45 N = 45
2.62 ± 0.59 2.60 ± 0.54
(IQR 2.25; 2.67; 3.00) (IQR 2.33; 2.67; 3.00)

(95% CI 0.01 – 0.07; P = 0.0004). The mean marginal
bone level at the last follow-up was 0.77 ± 0.22 mm
(95% CI 0.70 – 0.82). Thus, the mean marginal bone
loss experienced 30 months after initial loading was
0.60 ± 0.20 mm (95% CI 0.54 – 0.66; P < 0.0000;
Table 1).
The mean BOP values measured at the defini-
tive restoration delivery were 1.23 ± 0.93 (IQR
0.75; 1.00; 2.00), while 2 years afterwards they
were 1.17 ± 0.78 (IQR 1.00; 1.00; 2.00). The differ-
ence was not statistically significant (-0.06 ± 0.76;
P = 0.569).
The mean PPD values measured at the de-
finitive restoration delivery was 2.62 ± 0.59 mm
(IQR 2.25; 2.67; 3.00), while, 2 years after they
were 2.60 ± 0.54 mm (IQR 2.33; 2.67; 3.00).
The difference was not statistically significant
(-0.03 ± 0.62 mm; P = 0.765), (Table 2).
„ Discussion
The aim of this prospective study was to investigate
the 3-year clinical and radiographic data of one-
stage guided bone regeneration procedure, using a
layering technique consisting of a 2.0 mm-thick first
layer of particulated autologous bone on implant
threads and 2.0 mm of anorganic bovine to cover
the resorbed ridge, covered by a resorbable mem-
brane for horizontal augmentation of bony defects.
The main limitations of the present study were:
the relatively low number of patients, the relatively
short follow-up, the lack of a control group and the
self-assessment of failures and complications.
The results of this study confirm other reports
on the use of bone grafting materials and resorbable
membranes to treat horizontal defects, which may
lead to success when augmenting atrophic ridges9,15.
Autogenous bone block is still considered the first
choice for most reconstructive procedures5. Limi-
tations include additional operative time for graft
harvest, donor site morbidity, graft resorption, and
limited availability9. Numerous alternatives to bone
block graft have become available to address these
limitations. In accordance with the sandwich tech-
nique described by Wang et al16, in the present study
both materials have been used in two different lay-
ers, possibly combining the advantages of both with
collagen membranes17.
Non-resorbable e-PTFE membranes are consid-
ered the gold standard in GBR13,14, however, fre-
quently reported soft tissue complications, as well

Eur J Oral Implantol 2018;11(1):89–95


as the need to remove the membrane due to early
exposure, have led to the development and use
of resorbable membranes9. The lack of titanium
reinforcement in collagen membranes can be over-
come by an accurate fixation of the membrane that
allows a secure immobilisation of the graft material
until complete resorption of the membrane9,17. At
the best of our knowledge this is the only prospective
study with more than 2 years after loading follow-
up that evaluates the clinical outcome in accordance
with the sandwich technique first described by Wang
et al16. Therefore, our results could not be general-
ised and need to be confirmed by further prospective
studies. Moreover, the efficacy and the utility of the
two layers of bone need to be tested in RCTs compar-
ing the sandwich technique with the same approach
in one layer of anorganic bovine bone.
„ Conclusions
Within the limitation of the present study, the high
implant survival rate seems to validate the use of the
layer technique: 2.0 mm of particulated autologous
bone on implant threads and 2.0 mm of anorganic
bovine to cover all of the resorbed ridge, in combi-
nation with a resorbable membrane for horizontal
augmentation of horizontal bone width of between
4 mm and 6 mm. Further studies are needed to
evaluate the actual effectiveness of this technique.
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