Several grafting materials have been used in sinus augmentation procedures including autogenous bone, demineralized freeze-dried bone (DFDBA), hydroxyapatite, β-tricalcium phosphate (β-TCP), anorganic deproteinized bovine bone and combination of these and others. Up to now a subject of controversy in maxillofacial surgery and dentistry is, what is the most appropriate graft material for sinus floor augmentation.
Purpose
The aim of this study is to provide a body of evidence-based data regarding grafting materials in external sinus floor elevation concerning the fate of the augmented material at the histomorphological level, through a meta-analysis of the available literature.
Materials and methods
The literature searches were performed using the National Library of Medicine. The search covered all English and German literature from 1995 until 2006. For analyzing the amount of bone the parameter "Total Bone Volume" (TBV) was assessed. TBV is determined as the percentage of the section consisting of bone tissue.
Results
In a relatively early phase after implantation the autogenous bone shows the highest TBV values. Interestingly, the different TBV levels approximate during the time. After 9 months no statistically significant differences can be detected between the various grafting materials.
Conclusion
From a clinical point of view, the use of autogenous bone is advantageous if a prosthetic rehabilitation (with functional loading) is expected within 9 months. In other cases the use of anorganic deproteinized bovine bone in combination with autogenous bone seems to be preferable. Donor side morbidity is ignored in this conclusion.
The online version of this article (doi:10.1186/1746-160X-5-12) contains supplementary material, which is available to authorized users.
Competing interests
The authors declare that they have no competing interests.
Authors' contributions
JH conceived the study and drafted the manuscript. MS carried out the literature research. RD and CN calculated the statistics. MO, NK and UM participated in its design and coordination and helped to draft the manuscript. All authors read and approved the final manuscript.
Introduction
Since the external sinus floor elevation technique was first introduced by Boyne [1] and Tatum [2] several grafting materials have been used in sinus augmentation procedures including autogenous bone [1‐3], demineralized freeze-dried bone (DFDBA)[4, 5], hydroxyapatite [6], β-tricalcium phosphate (β-TCP) [7], anorganic deproteinized bovine bone [8] and combination of these and others [9]. Up to now a subject of controversy in maxillofacial surgery and dentistry exist, what is the most appropriate graft material for sinus floor augmentation. The consensus conference on sinus grafting held in 1996 showed that in the light of little data which are evidence-based many participants believed that autografts were the most efficacious [10]. However, the collection of autogeneous bone requires an extra donor site surgery and carries with it extra risks for morbidity and complaints, particularly when bone from the iliac crest is harvested [11]. According to Kent and Block [3] an ideal grafting material should fulfil the following criteria amongst other things:
Osteoinduction
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Osteoconduction
Volume stability
These criteria are best analysed by histological examinations. To the best of our knowledge, only a very small number of randomized controlled clinical trials have been conducted to compare various grafting materials with regard to these histological criteria. The available evidence therefore consists either of case reports, case series or retrospective studies. The aim of this study is to provide a body of evidence-based data regarding grafting materials in external sinus floor elevation to assist surgeons to make an informed choice between those materials, through a meta-analysis of the available literature.
Methods
The literature searches were performed using the National Library of Medicine (Internet: http://www.pubmed.com). The search covered all English and German literature from 1995 until 2006. Keywords used in the search were: "sinus" and "augmentation" and "bone substitute". The search was confined to studies or reports in humans. No animal studies were included. Moreover, review articles and in vitro studies were excluded. In all, 120 articles were identified and all abstracts were evaluated. After first evaluation the following inclusion criteria were added: The surgical procedure has to be an external sinus floor elevation and because of the presence of only single reports of some grafting materials – which does not allow a meta-analysis for those materials- the focus was on materials which are used in several studies/reports. Thus only papers using autogenous bone, demineralized freeze-dried bone (DFDBA), hydroxyapatite, β-tricalcium phosphate (β-TCP), anorganic deproteinized bovine bone (Bio Oss®, Geistlich Biomaterials, Wolhusen, Switzerland) [8] and combination of these materials were included. To standardize the multiple combinations of Bio Oss® with autogenous bone all mixing ratios higher than 80% Bio Oss® to 20% bone were pooled in the Bio Oss® group. Mixing ratios below (e.g. 50% Bio Oss® to 50% bone) were subsumed under the Bio Oss® + autogeneous bone group. Regarding the β-TCP group in almost all studies β-TCP was used without autogenous bone. In addition to review articles, interviews and editorials were excluded.
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For analyzing the amount of bone the parameter "Total Bone Volume" (TBV) was assessed. TBV is determined as the percentage of the section consisting of bone tissue [12]. This parameter was either directly taken from the paper or calculated where possible. In studies reporting woven and lamellar bone separately, the sum of both values was calculated whereas in studies determing lateral and central bone biopsies the mean was calculated.
For statistical analysis the data were weighted according to the number of observations in each study and the inverse variance. Moreover, to detect any statistical significant differences a weighted ANOVA with Random effect model and alpha-adjustment according to Tukey-Kramer for post hoc tests was used [13]. Differences were considered statistically significant if p < 0.05.
Results
After the initial literature search 120 articles were identified. Four of these articles were not written in English or german and another four were animal studies. Six articles were interviews or editorials and were excluded too. Of the remaining 106 articles 25 were not related to the external sinus floor elevation and another 16 articles gave an account on rare grafting material. Of the remaining 65 articles only in 30 studies the histomorphological parameter TBV was evaluable. That means that this parameter was explicitly noted in the article or could easily been calculated. Finally, only 30 articles remain for data analysis (table 1).
Table 1
Selection of evaluable articles by in- and exclusion criteria
Criteria
Studies which do not meet the criteria
Remaining studies
After initial literature search
120
English or german
4
116
Only human (no animal studies)
4
112
No interviews/editorials
6
106
Only external sinus floor elevation
25
81
Only autogenous bone, demineralized freeze-dried bone (DFDBA), hydroxyapatite, β-tricalcium phosphate (β-TCP), anorganic deproteinized bovine bone [8] and combination of these materials
16
65
TBV evaluable
35
30
In many of these 30 articles various grafting materials were described. In total 53 observations regarding grafting materials could be found. The vast majority were prospective studies, followed by some case reports or case series and finally one retrospective study (table 2).
Table 2
Distribution of articles and material observations
Σ
Case reports
Retrospective studies
Prospective studies
Studies
30
3
1
26
Examined grafting materials (in these studies)
53
4
3
46
A prerequisite for statistical analysis is that the mean values and the standard deviation is noted in the paper (criteria I) [13]. This is not the case in single case reports (criteria II). That is why those papers meeting one of these two criteria have to be excluded from further analysis (table 3). If a meta-analysis for one specific grafting material would be based on only one or two studies, the result would almost echo the findings of the single study. Therefore, it is rational to exclude materials with only one or two reports (criteria III). Table 3 shows the number of remaining studies/observations after application of these three criteria (Tab. 3). Finally, 30 articles remain for evaluation [7, 8, 12, 14‐41]. The studies are listed in table 4 (table 4). In no studies any allergic reactions to grafting materials or infections related to graft implantation were described.
Table 3
Selection of evaluable material observations by three exclusion criteria
Total observation
Criteria I: no mean value or SD
Criteria II: single case report
Criteria I or II
Remaining material observations
Algipore®
1
0
0
0
1
Bio Oss®
18
4
3
5
13*
Bio Oss® + autogen
(50:50 bis 80:20)
8
0
0
0
8*
DFDBA
1
1
0
1
0
HA
3
1
0
1
2
Autogen
13
3
5
4
9*
Autogen + DFDBA 50:50
1
0
0
0
1
Autogen + HA 50:50
1
0
0
0
1
β-TCP
7
1
1
1
6*
Σ
53
17
5
18
41 (36)
Note the numbers with * show the grafting materials with at least three reported observations (criteria III).
Table 4
List of reviewed publications.
Authors
Year of publication
Grafting material
Mean healing time (months)
n
TBV (%)
SD
Artzi Z. et al.
2001
BioOss
12.00
10
32.20
8.150
Artzi Z. et al.
2001
HA
12.00
10
42.10
10.010
Artzi Z. et al.
2002
BioOss
12.00
10
43.61
8.601
Artzi Z. et al.
2003
HA
12.00
10
32.95
7.991
Artzi Z. et al.
2005
BioOss
12.00
12
45.60
10.900
Artzi Z. et al.
2005
β-TCP
12.00
12
32.00
8.400
Boeck-Neto RJ. et al.
2002
autogen+DFDBA
10.00
5
50.46
16.290
Boeck-Neto RJ. et al.
2002
autogen+HA
10.00
5
46.79
8.560
Degidi M. et al.
2004
BioOss+autogen
6.00
12
38.80
3.200
Froum SJ. et al.
2002
BioOss
7.25
2
16.00
4.243
Froum SJ. et al.
2002
BioOss
11.00
1
32.00
.
Fugazotto PA. et al.
2003
BioOss
6.88
26
52.85
19.605
Fugazotto PA. et al.
2003
BioOss
12.50
5
68.80
7.400
Hallman M. et al.
2001
BioOss+autogen
7.00
16
24.70
16.901
Hallman M. et al.
2001
BioOss+autogen
30.00
12
50.70
22.800
Hallman M. et al.
2002
Autogen
12.50
11
37.70
31.300
Hallman M. et al.
2002
BioOss
14.75
10
39.90
8.000
Hallman M. et al.
2002
BioOss+autogen
12.50
11
41.70
26.600
John HD. et al.
2004
Autogen
5.50
4
53.50
2.520
John HD. et al.
2004
BioOss
5.50
21
29.52
7.430
John HD. et al.
2004
BioOss+autogen
5.50
13
32.23
6.860
Karabuda C. et al.
2001
BioOss
6.00
5
50.00
.
Karabuda C. et al.
2001
DFDBA
6.00
1
72.50
.
Karabuda C. et al.
2001
HA
6.00
3
27.50
8.660
Ozyuvaci H. et al.
2003
BioOss
7.00
44
47.50
0.945
Ozyuvaci H. et al.
2003
β-TCP
7.00
44
52.50
0.945
Proussaefs P. et al.
2003
BioOss
11.00
5
34.40
10.810
Scarano A. et al.
2004
BioOss
53.00
1
38.00
.
Schopper C. et al.
2003
Algipore
7.00
26
23.00
8.300
Szabo G. et al.
2001
Autogen
6.00
4
37.05
8.842
Szabo G. et al.
2001
β-TCP
6.00
4
29.37
10.568
Szabo G. et al.
2005
Autogen
6.00
20
38.34
7.400
Szabo G. et al.
2005
β-TCP
6.00
20
36.47
6.900
Tadjoedin ES et al.
2000
Autogen
5.00
9
42.28
3.251
Tadjoedin ES et al.
2000
Autogen
16.00
1
45.07
.
Tadjoedin ES et al.
2002
Autogen
5.00
2
40.05
1.061
Tadjoedin ES et al.
2002
Autogen
15.00
1
41.70
.
Tadjoedin ES et al.
2003
Autogen
5.00
1
37.30
.
Tadjoedin ES et al.
2003
BioOss
8.00
1
22.90
.
Tadjoedin ES et al.
2003
BioOss+autogen
6.33
3
29.57
4.508
Trisi P. et al.
2003
BioOss+autogen
15.33
9
44.38
8.575
Turunen T. et al.
2004
Autogen
6.75
14
25.10
7.200
Turunen T. et al.
2004
Autogen
13.75
4
25.10
6.300
Valentini P. et al.
2000
BioOss
6.00
3
21.08
7.250
Valentini P. et al.
2000
BioOss
12.00
3
27.55
4.880
Wallace SS. et al.
2005
BioOss
8.00
153
15.53
8.023
Yildrim M. et al.
2000
BioOss
7.00
11
14.70
5.000
Yildrim M. et al.
2001
BioOss+autogen
7.75
12
18.90
6.400
Zerbo IR. et al.
2001
β-TCP
8.00
1
20.00
.
Zerbo IR. et al.
2004
Autogen
6.00
5
41.00
10.000
Zerbo IR. et al.
2004
β-TCP
6.00
9
17.00
5.000
Zijderveld SA. et al.
2005
Autogen
6.00
5
41.00
10.000
Zijderveld SA. et al.
2005
β-TCP
6.00
9
17.00
5.000
n = number of patients
The weighted regression of TBV against the time point of sampling shows the development of the bone volume during time (Fig. 1). Interestingly, while Bio Oss®, Bio Oss® with autogenous bone and β-TCP show a steep increase the TBV of autogenous bone (without any additional grafting material) is decreasing. The increase of TBV during time in the Bio Oss® group can be considered as statistically significant.
×
Regarding Fig. 1 it is striking that there are two clusters of sampling. The first cluster comprise four until nine months after initial surgery and the second cluster span the time from nine months onwards. To compare the TBV depending on the grafting material the mean values were calculated for these two clusters. Because it is reasonable to weight the study results regarding the number of observations and the standard deviation both the "normal" and the adjusted mean values were calculated. In a relatively early phase after implantation the autogenous bone shows the highest TBV values. This was statistically significant (Fig. 2). Interestingly, the different TBV levels approximate during the time. After 9 months no statistically significant differences can be detected between the various grafting materials (Fig. 3). However, there was a strong tendency that Bio Oss® with autogenous bone shows the highest TBV values.
×
×
Discussion
External sinus floor augmentation has proven to be very effective in increasing bone volume in edentulous maxillary areas. Due to the significant resorption in the posterior maxilla following teeth extraction [42] there is often not enough bone volume to ensure the stability of dental implants [43]. Elevation and augmentation of the maxillary sinus can increase the bone height in the posterior area of the maxilla [1, 2]. Autogenous bone grafts obtained from the patient himself is very successful in bone regeneration and serves as a gold standard [10]. However, the explant of autogeneous bone requires an extra donor site surgery and is associated with an extra risks for morbidity and complaints, particularly when bone from the iliac crest is harvested [11]. Various bone grafting materials have been used as alternatives or supplements to autogenous bone such as demineralized freeze-dried bone (DFDBA), hydroxyapatite, β-tricalcium phosphate (β-TCP), anorganic deproteinized bovine bone [8] or combination of these materials. Bone grafting materials may produce bone formation by osteogenesis, osteoinduction or osteoconduction. Whereas osteogenesis is obtained by providing osteogenic cells and matrix directly in the graft (e.g. autogenous bone, distraction osteogenesis [44]), osteoinduction postulates that the grafted material is chemotactic to undifferentiated progenitor cells inducing them to differentiate into osteoblasts [31, 45]. Osteoconduction permits outgrowth of osteogenic cells from existing bone surfaces into the graft material [31]. Although these mechanisms have been described in detail, the question remains which bone grafting material is most suitable in external sinus floor augmentation at the histological level.
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One important finding of this study is that there is only little evidence for most of the grafting materials. Only anorganic deproteinized bovine bone (Bio Oss®) and pure-phase β-TCP (in most cases Cerasorb®, Curasan Pharma GmbH, Kleinostheim, Germany, was used) as well as autogenous bone (and combinations of these materials) were found to present evaluable data for meta-analysis. Interestingly, no reports regarding allergic reaction or infections caused by implantation of grafting material were described in the articles.
With regard to the TBV autogenous bone reaches the highest values during the first 9 months. This difference to the other materials was statistically significant. That's means that the percentage of mineralized bone was the highest. That is not surprisingly, because in the specimens of the other groups there are of course particles of the heterologous or alloplastic grafting material diminishing the percentage of the bone. Logically consistent the TBV shows the lowest values in the Bio Oss® and β-TCP groups. In contrast to this early phase there is no statistically significant difference between the grafting materials in the later phase anymore. Moreover, the values of the Bio Oss® group and Bio Oss® with autogenous bone show higher mean values than the pure autogenous bone, whereas the mean value of β-TCP is almost equal to autogenous bone. There could be two adverse effects after the initial grafting procedure. On the one hand bone is resorbed because in no case was any functional load on the grafting material (The samples of the patients were taken before the implant was in function). On the other hand the TBV in the Bio Oss® and β-TCP groups increased during time. That means that the grafting material is at least partially resorbed and replaced by bone. (Reduction of soft tissue volume hardly produce an increase of TBV because in sinus lift procedures soft tissue is very rare in the grafted material.) The first effect is well known and occurs in the alveolar bone usually after tooth extraction when the functional load is reduced or absent [42]. Additionally, there are reports in literature that up to 55% of the augmented autogenous bone resorbs during the first 6 months [46, 47]. The second effect reflects osteoinductive or at least osteoconductive properties of the non-autogenous grafting materials. Tadjoedin and colleagues describe in pure Bio Oss® grafts, that bone growth takes place through the guidance of osteogenic cells from existing bone surfaces of the grafted particles. This leads to the formation of woven bone between the grafted particles connecting them together into a mass of mineralized tissue [31]. When autogenous bone is mixed with Bio Oss® the human bone particles act as a source of bone cells [48, 49] providing more osteogenic cells and thus accelerating new bone formation. This is in line with an former study reporting that bone formation in a patient was faster in a mixed graft of Bio Oss® and autogenous bone than in a graft of Bio Oss® alone [50]. Bio Oss® seem to prevent bone loss and increase new bone formation but it is unclear wether or how fast the Bio Oss® particles will be resorbed. Both no resorption after six years [51] and slow resorption [31] are reported in literature.
In contrast to Bio Oss® there are reports that β-TCP is fully resorbed in 12 to 18 months and is replaced by bone that is similar both functionally and anatomically to the original bone [30]. Regarding the TBV there no statistically significant differences between Bio Oss® and β-TCP although the combination of Bio Oss® with autogenous bone shows the highest value in the later phase. Because β-TCP was used as a grafting material only without bone in the evaluated studies it might be that an additional supplement of autogeneous bone could increase the TBV too. The mechanism of preventing fast resorption and of increasing the TBV after about one year is probably very similar to Bio Oss®.
Conclusion
Taken together, comparability of Bio Oss® with or without autogenous bone and β-TCP to autogenous bone for sinus grafting can be regarded as evidence based concerning the histological bone structure after about 9 months. However, the augmented material contain more mineralized bone tissue 4–9 months after grafting when only autogenous bone is used. From a clinical point of view, the use of autogenous bone is advantageous if a prosthetic rehabilitation (with functional loading) is expected within 9 months. In other cases the use of Bio Oss® in combination with autogenous bone seems to be preferable. Donor side morbidity is ignored in this conclusion.
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When reviewing the literature and doing a meta-analysis there is one additional thing you have to bear in mind: the publication bias. That means that most of all authors report only from good results especially in case reports or case series. Bad or unwanted results are often neglected and not published in international journals. Therefore, even the results of this meta-analysis – although representing the highest grade of evidence – show presumably slightly to optimistic numbers.
Acknowledgements
We are very grateful to Dr. Reinhard Willers for his support in statistical analysis.
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Competing interests
The authors declare that they have no competing interests.
Authors' contributions
JH conceived the study and drafted the manuscript. MS carried out the literature research. RD and CN calculated the statistics. MO, NK and UM participated in its design and coordination and helped to draft the manuscript. All authors read and approved the final manuscript.
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