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YIJOM-4391; No of Pages 11

Int. J. Oral Maxillofac. Surg. 2019; xxx: xxx–xxx


https://doi.org/10.1016/j.ijom.2020.03.001, available online at https://www.sciencedirect.com

Pre-Implant Surgery

Volumetric osseous changes in R. Coopman1,2, J. Fennis1,


H. Ghaeminia1, G. Van de Vyvere3,
C. Politis2,4, T. J. M. Hoppenreijs1

the completely edentulous


1
Department of Oral and Maxillofacial
Surgery, Rijnstate Hospital, Arnhem,
Netherlands; 2Department of Oral and
Maxillofacial Surgery, University Hospitals

maxilla after sinus grafting and Leuven, Leuven, Belgium; 3Department of


Oral and Maxillofacial Surgery, Onze-Lieve-
Vrouw Ziekenhuis, Aalst, Belgium; 4OMFS–

lateral bone augmentation: a


IMPATH Research Group, Department of
Imaging and Pathology, Faculty of Medicine,
Catholic University Leuven, Leuven, Belgium

systematic review
R. Coopman, J. Fennis, H. Ghaeminia, G. Van de Vyvere, C. Politis, T. J. M.
Hoppenreijs: Volumetric osseous changes in the completely edentulous maxilla after
sinus grafting and lateral bone augmentation: a systematic review. Int. J. Oral
Maxillofac. Surg. 2019; xxx: xxx–xxx. ã 2020 International Association of Oral and
Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

Abstract. The aim of this systematic review was to evaluate the volumetric changes
associated with different bone grafting techniques in the completely edentulous
atrophic maxilla before dental implant placement. A search was performed
according to the PRISMA guidelines. A PICO question was formed, and the
PubMed, Scopus, Embase, and Cochrane Library databases were searched,
covering the period 2000–2018. Relevant data were extracted from the results
regarding study population, surgical details, technical information on volumetric
data acquirement, and volumetric outcome after bone augmentation procedures
before implant placement. Six articles with a combined population of 84 patients
were included. All patients had a completely edentulous maxilla, with a crestal
horizontal width of <3–4 mm or a crestal vertical height of <6–7 mm. The iliac
bone and ascending ramus were most frequently used as grafts. Five of the six
studies reported volumes of sinus inlay graft (SIG) and four reported volumes of
lateral bone augmentation (LBA). Radiographic analyses of the augmented areas
Key words: edentulous maxilla; maxillary atro-
differed among the studies. Volume loss after bone augmentation procedures ranged phy; bone graft; volumetric change; dental
from 5% to 50% for SIG and from 5% to 47% for LBA. All surgical augmentation implant.
techniques for the edentulous maxilla are prone to resorption; no procedure seemed
to be superior, but some interesting observations were made. Accepted for publication

Following the removal of teeth as a result of alveolar bone resorption, classified by and retention and loss of soft tissue support
infectious disease or trauma, the alveolar Cawood and Howell, can result in adverse of the upper lip, as well as having an impact
bone undergoes resorption. The process of effects, such as the loss of prosthetic support on vertical facial dimensions1–3.

0901-5027/000001+011 ã 2020 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Coopman R, et al. Volumetric osseous changes in the completely edentulous maxilla after sinus
grafting and lateral bone augmentation, Int J Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.ijom.2020.03.001
YIJOM-4391; No of Pages 11

2 Coopman et al.

Multiple surgical procedures have been The general conclusion throughout the cant advantage to partially edentulous
developed to improve the configuration of literature has been that all bone grafting patients in preventing occlusal stress on
the alveolar ridge in order to overcome procedures are prone to some resorption the grafts after LBA procedures. The im-
these adverse effects. Surgery can encom- before dental implant placement. Most of mobilization and fixation of LBA remains
pass procedures including the soft tissues the bone resorption and volumetric loss an important consideration in order to
(e.g., vestibuloplasty)4,5 and/or the bony takes place in the period immediately after allow vascular ingrowth within the graft
tissues, or refer to a dental prosthesis the augmentation procedure and before the and to enable osseoinduction21,22.
solution (e.g., sub-periosteal prosthesis)6. placement of dental implants14. The arguments above highlight that a
Historically, the use of soft tissue pro- Regarding the study population, it is completely edentulous study population
cedures has diminished due to the rise of difficult to assume that LBA for the place- seems to show different characteristics
dental implants. Dental implants in com- ment of a single implant in the anterior in comparison to a partially edentulous
bination with adequate prosthetics repre- region (regardless of the use of particu- study population. The aim of this system-
sent a major advancement in both lated or cortical bone) is comparable to a atic review was to evaluate the resorption
functional and aesthetic rehabilitation of SIG in a partially edentulous jaw or with rate of the augmented bone volume in the
the atrophic maxilla. An important prereq- the augmentation of a completely edentu- completely edentulous atrophic maxilla
uisite is the availability of a bony envelope lous jaw. Although a subpopulation with a from the moment of the surgical grafting
in which the dental implants can be completely edentulous maxilla has often procedure until dental implant placement.
placed. Another prerequisite is good pri- been included in major studies14–17, infor-
mary dental implant stability, which mation on volumetric changes after bone
requires an alveolar bone height of at least augmentation procedures in this patient Materials and methods
5 mm on average7. population, as a separate group, remains
Systematic literature search
When the alveolar process lacks these scarce.
minimal dimensions, bone augmentation Epidemiological studies have shown The English-language literature was
procedures can be considered. The main that total edentulism in comparison to searched for studies containing scientific
goal is to create a stable base for implant partial edentulism is associated with fac- data on volumetric changes of bone aug-
placement to restore dental and aesthetic tors such as low income, age, education, mentation procedures in the edentulous
functions prosthetically. Four types of and access to dental care18. With older maxilla. The search strategy was per-
maxillary reconstruction are usually de- age, changes in bone metabolism also formed according to the PRISMA (Pre-
scribed in the literature: sinus inlay grafts become a factor. Studies have shown that ferred Reporting Items for Systematic
(SIG), lateral bone augmentation (LBA)/ bone turnover and neovascularization is Reviews and Meta-Analyses) guide-
buccal onlay grafts, vertical onlay grafts, different in the elderly in comparison to lines23. Search strings with different sets
and interpositional grafts1,8–10 (Fig. 1). younger individuals19. According to Klijn of key words following the PICO criteria
Several studies and systematic reviews et al., an increase in patient age is associ- were formulated and used to search the
have been conducted to evaluate the qual- ated with a reduction in bone graft resorp- PubMed, Embase, Scopus, and Cochrane
ity of specific bone grafts and surgical tion20. Library databases. The PICO question was
procedures11–13. There is considerable The presence of occlusal relationships formulated as follows: P = patients with a
heterogeneity in the literature both in sur- in partially edentulous patients is another completely edentulous maxilla, I = bone
gical techniques and in study populations, reason for differentiating between patients augmentation procedure, C = not applica-
making the comparison of results between who are completely or partially edentu- ble, and O = volumetric bony changes
studies difficult. lous. Occlusal relationships give a signifi- from grafting procedure until dental im-

Fig. 1. Diagrams of the atrophic maxilla, depicting the different surgical procedures and definitions (left, frontal view; right, axial view).

Please cite this article in press as: Coopman R, et al. Volumetric osseous changes in the completely edentulous maxilla after sinus
grafting and lateral bone augmentation, Int J Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.ijom.2020.03.001
YIJOM-4391; No of Pages 11

Volumetric changes after sinus grafting 3

Fig. 2. Flowchart summarizing the search strategy, and the number of studies finally included in the analysis following the selection process using
the PubMed, Embase, Cochrane Library, and Scopus databases.

plant placement. The methodology and Study eligibility tulous population could not be uniformly
terms used in the search strategy are illus- extracted were excluded.
All studies had to meet the following
trated in Supplementary Material File 1.
inclusion criteria: (1) involve a study pop-
An extensive search was conducted
ulation of patients with a completely atro- Data extraction process
using the predetermined criteria. In the
phied edentulous maxilla, which could be
initial search, articles were selected based Two independent reviewers (R.C. and H.
classified as Cawood stage IV–VI; (2)
on title. After the removal of duplicates, G.) conducted the screening process for
history of surgical bone augmentation pro-
the abstracts of these articles were articles and reviewed the eligibility of
cedures performed in the completely eden-
screened. The remaining articles were retrieved articles. Any disagreement was
tulous maxilla: sinus inlay grafts (SIG),
investigated for relevance. The main fo- resolved by consultation with two addi-
lateral bone augmentation (LBA)/buccal
cus of the search was volumetric changes tional reviewers (T.H. and J.F.).
onlay grafts, vertical onlay grafts, inter-
after bone augmentation procedures for The following data were extracted from
positional grafts; (3) contains clear data
the edentulous maxilla. The references in the included studies: authors, year of pub-
about volumetric osseous changes after
each selected publication obtained from lication, population inclusion and exclu-
surgical augmentation procedures. The
the electronic search were screened man- sion criteria, surgical details, data
exclusion criteria were animal studies
ually to check for other eligible articles. concerning dental implants, technical in-
and publications not written in English.
The search was limited to studies in the formation on volumetric data acquire-
Many studies contained information about
English-language literature and those ment, and volumetric outcome after
volumetric changes after bone augmenta-
published between the year 2000 and bone augmentation procedures before
tion procedures in completely edentulous
December 2018. Radiographic volumet- dental implant placement. For some arti-
patients and partially edentulous patients
ric analysis studies published before 2000 cles, the corresponding author was con-
combined. Furthermore, many studies in-
were considered out of date. A final tacted to verify that the study population
cluded populations in which maxillae and
search of the literature was completed was completely edentulous and to supple-
mandibles were treated. Studies from
in December 2018. A flowchart summa- ment any missing data from the original
which the maxillary bone augmentation
rizing the search strategy is given in study. All articles were made consistent by
volumetric data from the completely eden-
Fig. 2. adjustment to the European metric system,

Please cite this article in press as: Coopman R, et al. Volumetric osseous changes in the completely edentulous maxilla after sinus
grafting and lateral bone augmentation, Int J Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.ijom.2020.03.001
YIJOM-4391; No of Pages 11

4 Coopman et al.

Table 1. Characteristics of the study populations.


Age (years)
Mean  SD
Author Population Median (range) Inclusion criteria Exclusion criteria Smoking
Dasmah et al. All: n = 11 NM Edentulous NM NM
(2012)29
M: n = 0 1. Ant: CVH <7 mm and/or CHW <3 mm
F: n = 11 2. Post: CVH <5 mm
Dreiseidler et al. All: n = 14 59  12 Cawood–Howell class IV, V, VI NM NDa
(2016)27
M: n = NM CVH <7 mm and/or CHW <6 mm
F: n = NM
Hernández- All: n = 14 51 (46–68) Edentulous: Cawood–Howell IV, V Smoking, Non-smoking, 14
Alfaro et al. previous
(2013)26 radiotherapy,
refusal to provide
written informed
consent
M: n = 4 1. Ant: CVH <6 mm and CHW <4 mm
F: n = 10 2. Post: CVH <6 mm
Johansson et al. All: n = 10 58 (49–71) Edentulous NM Non-smoking, 4
(2001)28
M: n = 3 1. Ant: Cawood–Howell IV Smokingb, 6
F: n = 7 2. Post: Cawood–Howell V, VI
Klijn et al. All: n = 20 Edentulous for 10 years NM NM
(2012)20
M: n = 8 M: 56  14
F: n = 12 M: 56  8
Xavier et al. All: n = 15 54  5 (48–60) Edentulous ASA 3 or 4, drug Non-smoking, 15
(2015)30 abuse, active
periodontitis in
the mandible
M: n = 8 Post: CVH <3 mm
F: n = 7
Ant, anterior; ASA, American Society of Anesthesiologists status; CBCT, cone beam computed tomography; CHW, crestal horizontal width;
CVH, crestal vertical height; F, female; M, male; ND, not described; NM, not mentioned; Post, posterior; SD, standard deviation.
a
Described but not distinguishable in the original study population27.
b
1–20 cigarettes/day.

with volume expressed in cubic centi- one of the domains was classified as hav- No studies on vertical bone augmenta-
metres (cm3). The coefficient of variation ing a moderate risk of bias. tion procedures or interpositional grafts
(CV) for the volume of interest (VOI) over could be included.
time was calculated using the following
formula: (Vn Vn 1)/Vn 1  100.
Results Population specifications
Both the volumetric measurements and
CV values were rounded up for compara- After the selection procedure, six articles The mean or median age of the study
bility between the different studies. describing six studies that met the inclu- population in all of the studies was >50
sion criteria remained. Two of these stud- years (Table 1). Overall, there were 84
ies were prospective26,27, two were patients in total, with a predominance of
Critical appraisal of individual studies retrospective20,28, and two were clinical female patients. The study populations
Two authors (R.C. and H.G) independent- trials29,30. The inclusion and exclusion consisted of patients with a completely
ly assessed the risk of bias for each study criteria of the populations were defined edentulous maxilla (Cawood–Howell
using the criteria proposed in the Meta- in all of the studies, as were the research classification of IV or higher) with a crest-
Analysis of Observational Studies in Epi- questions. No validated tool for measure- al horizontal width (CHW) <3–4 mm or
demiology statement24, Strengthening the ment of the data was reported in the crestal vertical height (CVH) <6–7 mm.
Reporting of Observational Studies in Epi- articles. Five studies had a high risk of One study included patients with
demiology statement25, and PRISMA bias and one study had a moderate risk of CVH < 3 mm30 (Fig. 1).
statement23. Any disagreements were re- bias (Supplementary Material, File 2).
solved by discussion or by involving two The two clinical trials had a split-mouth
design. After randomization, one side of Radiological volumetric analysis
additional authors (T.H. and J.F.) to adju-
dicate. When two or more domains were the maxilla (left or right) acted as the Volumetric data were acquired through
missing, the study was considered to have control site and the other as the test site. radiographic analysis (computed tomogra-
a high risk of bias. A study that included For both studies, the data for the control phy (CT) scan or cone beam CT (CBCT))
all domains was classified as having a low and test sites could easily be extracted and were expressed in cubic centimetres
risk of bias, whereas a study that lacked from the published results29,30. (cm3) (Table 2). Generally, three types of

Please cite this article in press as: Coopman R, et al. Volumetric osseous changes in the completely edentulous maxilla after sinus
grafting and lateral bone augmentation, Int J Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.ijom.2020.03.001
YIJOM-4391; No of Pages 11

Volumetric changes after sinus grafting 5

Table 2. Technical measurement specifications.


Author Radiographs Technical specifications Analysis Measurements
Dasmah et al. CT Pace Plus Distance axial 1. Number of investigators = 1 1. Manual linear
(2012)29 (General Electric, scans = 2 mm measurement of CVH,
USA) CHW, or CHL in selected
CT sections
Contiguous scan 2. Software: NM 2. Calculation mean for
CVH, CHW, and CHL
3. Manual search of 3 random CT 3.
sections (axial or coronal) each
showing the largest amount of bone
(test and control group) in all
dimensions
VOI = CVH  CHW  CHL
Dreiseidler et al. Galileos CBCT 512 pixels Resolution of 1. Number of investigators = NM Augmented areas outlined
(2016)27 (Sirona) 300 mm on axial scans and
multiplied by height
2. Software: SKY-PlanX (Bredent)
3. Automatic alignment of PE and
PO CBCT scan
Hernández- CBCT (i-CAT, 120 kV, 5 mA 1. Number of investigators = NM 1. VOI = volume caudal of
Alfaro et al. Imaging Sciences marked plane
(2013)26 International)
Axial slice distance 2. Software: SimPlant Pro Crystal 2. VOI calculated from
0.300 mm 3 (Materialise) ‘Mask list window’
SimPlant software
Field of view: 23 cm 3. Plane through both infra-orbital
foramina and spina nasalis
posterior
4. Modification of CBCT threshold
grey limits
Johansson et al. CT Pace Plus Distance axial 1. Number of investigators = 1 1. Threshold bone = HU
(2001)28 (General Electric, scans = 2 mm Contiguous >150
USA) scan
2. Scan parallel to palatal plane 2. VOI = S
(CHW  CHL  2 mm)a
3. Software: 9.0 Denta2 Scan
Klijn et al. CBCT (i-CAT, 120 kV, 3–8 mA (pulse 1. Number of investigators = 1 1. Threshold = grey value
(2012)20,b Imaging Sciences mode) >110
International)
Focal spot: 0.5 mm 2. Software: CT-Analyzer V1.10 2. Augmented area
manually drawn through
consecutive coronal
sections
Field of view: 16  22 cm 3. Reslicing in coronal sections Software calculated VOI
(section thickness 0.265 mm)
Voxel size: 0.4 mm 3
Xavier et al. CBCT (i-CAT, 0.25 mm slice 1. Number of investigators = NM VOI = NM
(2015)30 Imaging Sciences reconstruction
International)
2. Software: Mimics 8.13
CBCT, cone beam computed tomography; CHL, crestal horizontal length; CHW, crestal horizontal width; CT, computed tomography; CVH,
crestal vertical height; HU, Hounsfield units; NM, not mentioned; PE, preoperative; PO, postoperative; VOI, volume of interest.
a
Additional information acquired from former publications by the same author.
b
Additional information acquired through e-mail contact with the corresponding author.

VOI calculation could be defined (Fig. 3A- length (CHL). Only the sections showing Belgium): the VOI was the maxillary
–C, Table 2). the largest amount of bone in all dimen- volume caudal to the marked plane
The most frequently used method was sions were used. The mean values were through both the infra-orbital foramina
outlining the augmented area on the CT calculated for CVH, CHW, and CHL, and spina nasalis posterior (Fig. 3C)26.
scan for each consecutive slice20,27,28. based on three measurements. The VOI This was the only research group to
Nonetheless, all authors used different was calculated by computing the three report a preoperative volume of the max-
types of parameters in comparison to each mean values, resulting in a volumetric illa; on the other hand, no clear division
other (Fig. 3A). rectangle (Fig. 3B)29. could be made between LBA and SIG
One study group selected three random Another research group used a procedures.
CT axial and coronal sections showing the completely different third approach, ap- The final group used Mimics software
largest CVH, CHW, and crestal horizontal plying SimPlant software (Materialise, (Materialise, Belgium) to calculate the

Please cite this article in press as: Coopman R, et al. Volumetric osseous changes in the completely edentulous maxilla after sinus
grafting and lateral bone augmentation, Int J Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.ijom.2020.03.001
YIJOM-4391; No of Pages 11

6 Coopman et al.

Data on SIG procedures are reported in


Table 3; five of the six studies reported
volumetric data for SIG. Two of studies
reported data on particulated autogenous
bone grafts (PAG) of the iliac bone (IBG).
One of these studies reported an average
volume loss of 1.1 cm3 at 6 months post-
operative, with a CV of 50%28. The
other study reported an average volume
loss of 0.4 cm3 and CV of 25% at 4
months postoperative20. Both studies de-
scribed similar surgical techniques and
methods of VOI calculation20,28.
One study reported SIG procedures with
PAG of autogenous IBG mixed with plate-
let-rich plasma (PRP). These procedures
resulted in a VOI loss at 6 months post-
operative of 1.5 cm3 at the test site and
2.0 cm3 at the control site. The reported
CV were 33% and 42%, respective-
ly29.
PAG of autogenous ascending ramus
grafts (ARG) showed an average volume
loss of 0.5 cm3, or a CV of 24% at 6
months postoperative30. The VOI loss af-
ter augmentation with an allogeneic distal
femur head (DFH) graft was 0.7 cm3 in the
first 6 months postoperative, with a CV of
30%30.
Autogenous ARG mixed with deminer-
alized bovine bone particles (DBBP)
showed a VOI loss of 1 cm3 and a CV
of 5% at 3–4 months postoperative26.
Data concerning LBA procedures are
described in Table 4. Only four of the six
studies reported volumetric data on the
LBA (Table 4). A monocorticocancellous
bone block fixed with miniscrews (CCB-
FMS) was used in all cases except in the
test group in the study by Dasmah et al.29.
In that study, CCB-FMS (n = 11) was
Fig. 3. (A) Volume of interest (VOI) calculation according to Johansson et al.28 (2002). The compared with a LBA technique consist-
outline of the sinus inlay graft and lateral bone augmentation graft on each scan was plotted and ing of a PAG mixed with PRP (n = 11).
the area calculated automatically. The VOI was calculated by multiplying these areas by the Three studies reported data on the au-
height of each radiographic slice (2 mm). (B) VOI calculation according to Dasmah et al.29 togenous IBG fixed with a miniscrew as
(2012). Three schematic diagrams of different CT sections (axial and sagittal) are depicted,
the monocorticocancellous bone block
showing the maximum amount of bone in all dimensions. The crestal horizontal length (CHL),
crestal horizontal width (CHW), and crestal vertical height (CVH) were measured. The mean (CCB-FMS). One study reported an aver-
value was calculated for each dimension, and the values were multiplied to obtain the VOI. (C) age volume loss of 1.1 cm3 and CV of
VOI calculation according to Hernández-Alfaro et al.26 (2013). A plane was delineated using the 47% at 6 months postoperative28, anoth-
posterior nasal spine and both infraorbital foramina as anatomical landmarks. The VOI was er an average volume loss of 0.4 cm3 and
defined below this plane until the inferior limit of the residual alveolar ridge. CV of 17% at 4 months postoperative27,
and the final one an average volume loss of
1.8 cm3 and CV of 37% at 6 months
VOI, but no further details were men- local anaesthesia with or without intrave- postoperative29. All studies described sim-
tioned30. nous sedation. Antibiotics used were peni- ilar surgical techniques and methods of
cillins (benzyl-, phenoxymethyl-, or VOI calculation27–29.
aminopenicillin) or clindamycin (Tables The LBA procedures in the clinical trial
Volumetric changes according to the
3 and 4). test group (Dasmah et al.29), consisting of
surgical procedure performed
Postoperative radiographic scans were PAG of autogenous IBG mixed with PRP,
The autogenous iliac bone graft (IBG) was performed during the first weeks. A sec- resulted in a VOI loss of 3.2 cm3. The
the most common donor graft for recon- ond radiological follow-up was done on reported CV was 67% at 6 months post-
struction of the edentulous maxilla (Tables average between 4 and 6 months after the operative29. The resorption rate for LBA
3 and 4). The bone graft surgery was initial augmentation procedures before differed markedly between LBA of par-
performed under general anaesthesia or dental implantation (Tables 3 and 4). ticulate bone mixed with PRP and LBA

Please cite this article in press as: Coopman R, et al. Volumetric osseous changes in the completely edentulous maxilla after sinus
grafting and lateral bone augmentation, Int J Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.ijom.2020.03.001
YIJOM-4391; No of Pages 11
Table 3. Surgical specifications—focus on sinus inlay grafts (SIG).
grafting and lateral bone augmentation, Int J Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.ijom.2020.03.001
Please cite this article in press as: Coopman R, et al. Volumetric osseous changes in the completely edentulous maxilla after sinus

Sinus inlay graft (SIG) procedures Population Study Surgical specifications Interval radiographs Changes in VOI Coefficient of variation (CV)
3
Graft: autogenous IBG Maxilla, n = 10 Johansson et al. General anaesthesia No preoperative X-ray V1 = 2.3 cm (SD 0.8) CV 6 months: 50%
(2001)28
3
Recipient: PAG Sinus, n = 20 Incision: NM Post-augmentation (V1) V2 = 1.2 cm (SD 0.6)
Antibiotics: yes (10 days) Pre-implantation (V2)
DFP: 4–6 weeks
Graft: autogenous IBG Maxilla, n = 20 Klijn et al. General anaesthesia Preoperative X-ray V1 = 1.7 cm3 (SD NM) CV 4 months: 25%
(2012)20
Recipient: PAG Sinus, n = 38 Incision: crestal, full- Post-augmentation (V1) V2 = 1.3 cm3 (SD NM)
thickness
Antibiotics: yes (7 days) Pre-implantation (V2)
DFP: 3–4 weeks
Graft: autogenous ARG Maxilla, n = 15 Xavier et al. Local anaesthesia Preoperative V1 = 2.0 cm3 (SD 0.4) CV 6 months: 24%
(2015)30 –
Control site
Recipient: PAG Sinus, n = 15 Incision: crestal, full Post-augmentation (V1) V2 = 1.5 cm3 (SD 0.5)
thickness, two vertical
releasing incisions
Antibiotics: yes (PE) Pre-implantation (V2)
DFP: NM
Graft: allogenic DFH (FFB) Maxilla, n = 15 Xavier et al. Local anaesthesia Preoperative V1 = 2.5 cm3 (SD 0.8) CV 6 months: 30%
(2015)30 – Test
site
Recipient: PAG Sinus, n = 15 Incision: crestal, full Post-augmentation (V1) V2 = 1.8 cm3 (SD 0.6)
thickness, two vertical
releasing incisions
Antibiotics: yes (PE) Pre-implantation (V2)
DFP: NM
Graft: autogenous IBG Maxilla, n = 11 Dasmah et al. General anaesthesia No preoperative X-ray V1 = 4.8 cm3 (SD 1.8) CV 6 months: 42%
(2012)29 –
Control site
Recipient: PAG mixed with PRP Sinus, n = 11 Incision: NM Post-augmentation (V1) V2 = 2.8 cm3 (SD 1.0)

Volumetric changes after sinus grafting


Antibiotics: yes Pre-implantation (V2)
DFP: 1 month
Graft: autogenous IBG Maxilla, n = 11 Dasmah et al. General anaesthesia No preoperative X-ray V1 = 4.5 cm3 (SD 1.9) CV 6 months: 33%
(2012)29 – Test
site
Recipient: PAG mixed with PRP Sinus, n = 11 Incision: NM Post-augmentation (V1) V2 = 3.0 cm3 (SD 1.7)
Antibiotics: yes Pre-implantation (V2)
DFP: 1 month
Graft: autogenous ARG and DBBP Maxilla, n = 14 Hernández- IV sedation and general Preoperative V0 = 11.3 cm3 (SD 2.3) CV 4 months: 5%
Alfaro et al. anaesthesia
(2013)26
Recipient: PAG mixed with DBBP Sinus, n = 28 Incision: crestal, full- Post-augmentation (V1) V1 = 20.0 cm3 (SD 2.9)
thickness
Antibiotics: yes (7 days) Pre-implantation (V2) V2 = 19.0 cm3 (SD 2.4)
DFP: 1 week
ARG, ascending ramus graft; DBBP, demineralized bovine bone particles (Bio-Oss); DFH, distal femur head; DFP, denture-free period; FFB, fresh frozen bone; IBG, iliac bone graft; IV, intravenous;
NM, not mentioned; PAG, particulated autogenous graft; PE, preoperative; PRP, platelet-enriched plasma; SD, standard deviation; VOI, volume of interest.

7
8

YIJOM-4391; No of Pages 11
Table 4. Surgical specifications—focus on lateral bone augmentation (LBA).
grafting and lateral bone augmentation, Int J Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.ijom.2020.03.001
Please cite this article in press as: Coopman R, et al. Volumetric osseous changes in the completely edentulous maxilla after sinus

Lateral bone augmentation

Coopman et al.
(LBA) procedures Population Study Surgical specifications Interval radiographs Changes in VOI Coefficient of variation (CV)
Graft: autogenous IBG Maxilla, n = 10 Johansson et al. General anaesthesia No preoperative X-ray V1 = 2.3 cm3 (SD 1.2) CV 6 months: 47%
(2001)28
Recipient: CCB-FMS Sinus, n = 20 Incision: NM Post-augmentation (V1) V2 = 1.2 cm3 (SD 0.8)
Antibiotics: yes (10 days) Pre-implantation (V2)
DFP: 4–6 weeks
Graft: autogenous IBG Maxilla, n = 16 Dreiseidler et al. General anaesthesia No preoperative X-ray V1 = 2.5 cm3 (SD 1.3) CV 4 months: 17%
(2016)27
Recipient: CCB-FMS Incision: high in Post-augmentation (V1) V2 = 2.1 cm3 (SD 1.2)
vestibular gingiva
Antibiotics: yes Pre-implantation (V2)
DFP: NM
Graft: autogenous IBG Maxilla, n = 11 Dasmah et al. General anaesthesia No preoperative X-ray V1 = 4.8 cm3 (SD 1.0) CV 6 months: 37%
(2012)29 –
Control site
Recipient: CCB-FMS Control, n = 11 Incision: NM Post-augmentation (V1) V2 = 3.0 cm3 (SD 1.5)
Antibiotics: yes Pre-implantation (V2)
DFP: 1 month
Graft: autogenous IBG Maxilla, n = 11 Dasmah et al. General anaesthesia No preoperative X-ray V1 = 4.8 cm3 (SD 1.5) CV 6 months: 67%
(2012)29 – Test
site
Recipient: PAG mixed with PRP Test, n = 11 Incision: NM Post-augmentation (V1) V2 = 1.6 cm3 (SD 0.6)
Antibiotics: yes Pre-implantation (V2)
DFP: 1 month
Graft: autogenous ARG and Maxilla, n = 14 Hernández- IV sedation and general Preoperative V0 = 11.3 cm3 (SD 2.3) CV 4 months: 5%
DBBP Alfaro et al. anaesthesia
(2013)26
Recipient: CCB-FMS, DBBP, Sinus, n = 28 Incision: crestal, Post-augmentation (V1) V1 = 20.0 cm3 (SD 2.9)
RCM full-thickness
Antibiotics: yes (7 days) Pre-implantation (V2) V2 = 19.0 cm3 (SD 2.4)
DFP: 1 week
ARG, ascending ramus graft; CCB-FMS, monocorticocancellous bone block fixed with miniscrews; DBBP, demineralized bovine bone particles (Bio-Oss); DFP, denture-free period; IBG, iliac bone
graft; IV, intravenous; NM, not mentioned; PAG, particulated autogenous graft; PRP, platelet-enriched plasma; RCM, resorbable collagen membrane (Bio-Gide); SD, standard deviation; VOI, volume
of interest.
YIJOM-4391; No of Pages 11

Volumetric changes after sinus grafting 9

with a monocorticocancellous iliac bone statement confirmed by most authors of cence and interference from wound irrita-
graft at 6 months postoperative29. the included studies26–28. tion or friction, reducing micromovements
The use of an autogenous ARG bone Overall, the methods described provid- of the bone grafts.
block added with xenografts (DBBP cov- ed a clear description of how to calculate One research group used collagen bar-
ered with a resorbable collagen mem- the VOI. The method used by Dasmah rier membranes26. Based on the present
brane) showed a VOI loss of 1 cm3 and et al. (Fig. 3B) is effective for comparing data (mainly due to the different method of
a CV of 5% at 3–4 months postopera- two surgical protocols in the same patient, calculation of the VOI), it is difficult to
tive26. but seemed to overestimate the real vol- draw firm conclusions on the use of mem-
For the comparison of SIG with LBA ume of bone compared with the other branes. Gielkens et al. concluded that the
procedures, two studies provided useful studies29. By taking the mean of the larg- added value of these membranes in pre-
data28,29. In the first study, the rate of est CVH, CHW, and CHL, a volumetric venting bone resorption in the completely
volume loss did not differ much between rectangle is measured; in reality, the bone edentulous maxilla is still debatable. The
SIG and LBA ( 50% vs 47%)28. In the graft has a more elliptic shape, so the potential benefits of using either resorb-
second study, volume loss at the SIG sites volume of the real augmented volume able or non-resorbable barrier membranes
(with CV 33% and 42%) differed from block is overestimated in comparison with do not overcome the risk of exposure
that at the LBA sites (CV of 37% for the data reported in the other studies. during the healing period and subsequent
CCB-FMS and 67% for PAG mixed Hernández-Alfaro et al. evaluated treat- complications34.
with PRP)29. ment outcomes with volume-rendering With regard to the SIG procedures (Ta-
software tools for CBCT, allowing a stan- ble 3), data for the studies using autoge-
dardized three-dimensional analysis of the nous IBG showed that the volume loss in
Discussion
results (Fig. 3C)26. It should be mentioned the study by Klijn et al.20 was half the
Population specifications that by making a two-dimensional plane volume loss reported by Johansson et al.28
through the infra-orbital foramen and pos- (CV 25% vs 50%). Both studies used
Over the decades, increasing evidence has
terior nasal spine, the zygomas are partial- the same technical and surgical methods,
suggested that the causative pathology
ly considered in calculations of the VOI. except the time to dental implantation.
differs between partially edentulous
The method described seems to be one of The discrepant results reported by Klijn
patients and those who are completely
the quickest means of obtaining preopera- et al. could be explained by the smaller
edentulous (caries, trauma versus peri-
tive and postoperative volumetric data. augmented bone volume used, or the fact
odontal diseases as the cause of dental
The study by Hernández-Alfaro et al. that the study population was edentulous
loss)18,31,32. Also, occlusal stability and/
was the only one to provide preoperative for more than 10 years, making additional
or dental support is an important differ-
volumetric data. post-extraction resorption of the alveolar
ence when considering pressure forces on
process less acceptable20.
different bone augmentation techniques
Another study (Dasmah et al.29), with a
between partially and completely edentu- Volumetric changes according to the
different technical method, also reported
lous patients. Therefore, the decision was surgical procedure performed
volumetric data on SIG with autogenous
made to include only study populations
No studies that met the inclusion criteria IBG. The raw volume data were not com-
with a completely edentulous atrophic
reporting data on vertical augmentation parable to those of the former studies, but
maxilla.
procedures or interpositional grafts were the CV values were located in between
Although a limited number of articles
found. The preferred procedures were SIG ( 33% and 42%).
met the inclusion criteria, the mean age of
and LBA. The distinction between these The volumetric data of SIG with ARG
the study population and the initial dimen-
techniques was made for comparability of or allogeneic DFH were comparable to
sions of the alveolar ridge (CHW and
the results. Otherwise, both procedures are those of the previously mentioned studies,
CVH) were comparable throughout. The
difficult to separate in the restoration of an and no major differences in the CV values
predominance of female patients in the
edentulous maxilla, and should be seen were noted between the allografts and
study populations was notable. A short-
surgically as one entity. autografts30.
coming of all of the included articles was
The preferred donor sites were the an- The lack of baseline CBCT or CT scans
the small size of the study populations,
terior iliac crest (IBG) and the mandibular makes it difficult to compare the initial
which makes detecting differences among
ascending ramus (ARG) (Tables 3 and 4). situations between the aforementioned
them difficult.
No published studies with a completely authors. Uchida et al. (1998), in a study
edentulous population reporting volumet- involving a group of partially edentulous
ric data on calvarial or chin bone grafts patients, reported that the inferior portions
Radiological volumetric analysis
were found. The latter is possibly of the sinus measured on CT images were
The use of CBCT has offered enormous explained by a discrepancy in the amount 0. cm3 for 5-mm lifting and 1.9 cm3 for
advantages in dose reduction, availability, of graft volume necessary and the amount 10-mm sinus floor elevation35, which cor-
and costs, leading to rapid and clear indi- available to harvest in the interforaminal responds with the data reported above.
vidual data acquisition. The main disad- area. Some authors preferred allografts, Based on the present data, it seems that
vantage of CBCT is the absence of which have the advantage that no donor no type of graft can be preferred over
Hounsfield units, which makes it difficult site is necessary30. Nevertheless, allo- another with regard to volumetric osseous
to compare images in a validated way33. grafts have been plagued by their unpre- changes over time.
Due to recent changes and dose reductions dictable rates of resorption, bone Data on LBA procedures (Table 4)
in the field of CT scans, micro-CT might formation, and infection rate22. showed that an autogenous monocortico-
represent a future alternative. It appears A denture-free period (1–4 weeks) en- cancellous bone block was fixed with a
that no validation study has compared the sured good healing of the mucoperiosteal miniscrew to the maxilla in three studies.
different methods of VOI calculation, a flap. This healing prevented wound dehis- The resorption rate or CV varied from

Please cite this article in press as: Coopman R, et al. Volumetric osseous changes in the completely edentulous maxilla after sinus
grafting and lateral bone augmentation, Int J Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.ijom.2020.03.001
YIJOM-4391; No of Pages 11

10 Coopman et al.

17%27 to 37%29 and 47%28. The relative proportions of cortical and cancel- trends are noted but no firm evidence
vestibular incision in the mobile mucosa lous bone within the graft. The microarch- exists to favour one augmentation proce-
used by Dreiseidler et al. may result in less itecture of a bone graft is perhaps the most dure over the other, due to different radio-
wound tension, leading to fewer infectious important determinant of graft volume logical analyses.
complications27. This incision could ex- maintenance39. The characteristics of the
plain the lower resorption rate of the soft tissue envelope at the recipient site
grafted volume in comparison to the other and the position in which the graft is Funding
studies27–29. placed (i.e., inlay vs. onlay) dictate the No funding to declare.
LBA reconstruction with particulated mechanical forces on the grafted bone. In
IBG mixed with PRP showed significantly essence, the form of a bone follows its
more resorption in comparison to CCB- function (Wolff’s law). Morphogenetical- Competing interests
FMS29. Autologous bone blocks still ap- ly, many different types of bone substitute No conflict of interest to declare.
pear to be the most reliable and secure can be used to supply the material needed
procedure for LBA in the case of extreme for the procedure, e.g., autologous, allo-
resorption36. geneic grafts, xenograft, or alloplastic Ethical approval
The autogenous ARG bone block added materials. Not required.
with xenografts (DBBP) and covered with Alveolar bone resorption occurs after
a resorbable collagen membrane showed a tooth extraction, and in all of the included
mean augmentation of 9 cm3 in LBA and studies, bone grafting procedures were Patient consent
SIG procedures, and a CV of 5%26. The also prone to resorption. The concept of
Not required.
autogenous ramus graft could represent an the biological tissue envelope states that
alternative intraoral donor site, with less the bone form follows function40,41. Con-
morbidity than with anterior iliac grafts26. sequently, if the bone is not functional, it Acknowledgements. Benjamin De Maere
By adding the volume of the zygomas in will resorb, or if bone is too extensively for the illustrations.
the VOI calculation, the actual resorption present, the functionality (e.g., by dental
was underestimated compared to the other implants) in its environment will return it
methods, because the initial volume was to its original dimensions.
relatively larger. Other authors have also The primary goal of a bone grafting Appendix A. Supplementary data
suggested that the envelopment of the procedure is to create a stable bony base
autogenous grafts with DBBP could re- to facilitate the surgical placement of den- Supplementary material related to this
duce resorption of the autograft37. tal implants. Grafting solutions can pro- article can be found, in the online version,
When comparing SIG with LBA proce- vide a less prosthetically demanding at doi:https://doi.org/10.1016/j.ijom.2020.
dures, it has been postulated that the re- scenario because the alveolar anatomy is 03.001.
construction with an onlay graft (LBA) is restored. This systematic review describes
more prone to resorption than the recon- multiple surgical ways to achieve this
struction with an inlay graft (SIG); this goal. References
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Please cite this article in press as: Coopman R, et al. Volumetric osseous changes in the completely edentulous maxilla after sinus
grafting and lateral bone augmentation, Int J Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.ijom.2020.03.001
YIJOM-4391; No of Pages 11

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Please cite this article in press as: Coopman R, et al. Volumetric osseous changes in the completely edentulous maxilla after sinus
grafting and lateral bone augmentation, Int J Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.ijom.2020.03.001

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