rio N. Favato Ma Bruno C.L. Vidigal Maurıcio G. Cosso vio R. Manzi Fla Jamil A. Shibli bio Elton G. Zeno
Impact of human maxillary sinus volume on grafts dimensional changes used in maxillary sinus augmentation: a multislice tomographic study
Authors’ affiliations: M ario N. Favato, Maurıcio G. Cosso, Elton G. Zen obio, Department of Dentistry, Implant Master Program, PUCMINAS, Belo Horizonte, Brazil Bruno C.L. Vidigal, Fl avio R. Manzi, Department of Dentistry, Radiology Master Program, PUCMINAS, Belo Horizonte, Brazil Jamil A. Shibli, Department of Periodontology and Oral Implantology, UNG, Guarulhos, Brazil
Key words: Sinus lift, Bone formation, Sinus volume, Biomaterial, Multislice tomography
Corresponding author: Elton Goncßalves Zen obio Department of Dentistry Implant Master Program Av. Dom Jos e Gaspar – 500, 46 Hall CEP – 30535.610, Belo Horizonte, Brazil. Tel.: +55 31 33194414 Fax: +553133194410 e-mail: [email protected]
Abstract Purpose: To assess the influence of complete maxillary sinus volume on the dimensional changes of different grafts used in maxillary sinus lift. Materials and Methods: Analysis of 50 surgical procedures of maxillary sinus lift performed on 43 subjects using different grafting materials: fresh frozen allogenic particulated bone (11), hydroxyapatite (Endobonâ) (17), 60% hydroxyapatite + 40% beta-tricalcium phosphate (Bone Ceramicâ) (12) and Bone Ceramicâ + Emdogainâ (10). One hundred and fifty multislice tomographic images of the maxillary sinus were obtained using the software Syngo CT 2011 A VOLUME, measuring complete maxillary sinus volume (T0) and dimensional changes of different graft materials during periods of 15 days (T1) and 180 days (T2). The factor studied was the influence of maxillary sinus volume on the dimensional changes of different graft materials used in maxillary sinus lift in patients with posterior edentulism. Data obtained were assessed using the Student’s t-test and Pearson’s correlation coefficient. Results: No correlation (r 0.112) between the total maxillary sinus volume and the dimensional changes of the different graft materials used in this study was observed (P > 0.05). Conclusion: This study demonstrated that there is no sufficient evidence to support the thesis that the volume of the maxillary sinus influences the contraction of the grafts, at least on sample or the biomaterials evaluated in this cohort study.
Date: Accepted 27 August 2014 To cite this article: Favato MN, Vidigal BCL, Cosso MG, Manzi FR, Shibli JA, Zen obio EG. Impact of human maxillary sinus volume on grafts dimensional changes used in maxillary sinus augmentation: a multislice tomographic study. Clin. Oral Impl. Res. 26, 2015, 1450–1455 doi: 10.1111/clr.12488
1450
The maxillary sinus is the largest of all paranasal sinuses: pyramidal shaped, with approximate dimensions of 20 mm length, 40 mm height and 30 mm depth (Emtiaz et al. 2006). Authors have suggested some hypotheses about the functions of the maxillary sinus (Blanton & Biggs 1969): moistening inspired air; expanding the area of the olfactory membrane; absorbing direct impact to the skull structure; secreting mucus to humidify the nasal cavity; insulating the brain thermally; contributing to facial growth; and decreasing the weight of the skull. At six years of age, the cavity starts to take the pyramidal shape and becomes radiographically visible. Maxillary sinus volume has a fast growth rate in children up to 12 years of age, after which its growth rate decreases and becomes stable after the eruption of the last molars (Maresh 1940; Abubaker 1999).
Dental loss induces maxillary sinus expansion, possibly creating a union between the sinus floor and the crest of the remaining alveolar ridge (Misch 2008). This expansion is related to sinus height and length, rather than depth (Uchida et al. 1998). After tooth extraction, a 25% decrease is observed in ridge volume during the first year, reaching 40–60% in length during the first three years (Misch 2008). Lateral access sinus augmentation technique has been widely studied and described as a safe and highly predictable treatment (Similer et al. 1992; Zinner & Small 1996; Block et al. 1998; Pjetursson et al. 2008). To assess bone-grafting procedures in maxillofacial reconstructive surgeries, it is important to have reliable and accurate diagnostic methods, capable of determining the longitudinal survival of bone grafts. In this context,
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Favato et al Maxillary sinus volume and graft changes
three-dimensional computerized tomography (3D CT scan) assesses the correlation between the real volume measurements of bone grafts and the volumes measured by the 3D CT scan, to determine the accuracy of this type of examination (Jensen et al. 1997). Uchida et al. (1998) determined the maxillary sinus volume and took it as a reference to define the volume of bone graft needed to allow further implant placement. Taking into account the individual differences in terms of maxillary sinus volume and the resorption of grafted materials, an approximate volume of 5.46 cm3 was needed for a 15-mm lift and approximately 7.96 cm3 for a 20-mm lift. Studies report results regarding the volumetric stability of different materials used in maxillary sinus lift for further osseointegrated implant placement (Chart 1). It has been reported that the higher the residual bone, the greater the success rate, regardless of whether one- or two-stage approaches were used (Jensen & Greer 1992; Geurs et al. 2001; Peleg et al. 2006; Mardinger et al. 2007; Rios et al. 2009). The low percentage of new bone formation in three patients (17%) can be partly explained by the presence of very extensive nasal cavities, either in the mesial–distal or buccal–palatal directions. Larger maxillary sinuses may present reduced osteogenic potential as a result of the distance between the source of osteogenic cells and the peripheral angiogenesis. Therefore, from the biological standpoint, they merely assumed that the larger volume of maxillary sinus determines a greater graft contraction and a longer new bone formation time (Kolerman et al.2008). Soardi et al. (2011), in human histological assessments of mineralized bone graft to maxillary sinus floor elevation (ridge height 15 mm. Results of this study demonstrated that of the 15 sinuses classified as large, two required a longer maturation period to attain an adequate amount of newly formed bone. Despite the different studies about the volumetric stability of different grafting materials for sinus floor lifting procedures (Wanschitz et al. 2006; Kirmeier et al. 2008; Arasawa et al. 2012; Klijn et al. 2012; Cosso et al. 2013; Kim et al. 2013; Sbordone et al. 2013; Umanjec-Korac et al. 2013) none of them has assessed the influence of the total volume of the sinus in the shrinkage of grafted materials. Perhaps, these theories (Gray et al. 2001; Jonhansson et al. 2001), about the relationship of the influence of the graft volume dimensional changes, materials characteristics and the total volume of maxillary sinus have not yet been clarified.
Images analysis
A 128 multislice tomography was used to capture the images (Somatom, Siemens, Erlangen, Germany). Multislice tomographic images were used to assess the mass volume of the sinus lift grafts as a way to measure the degree of volume alteration between the two healing stages. The software Siemens SOMATOM, Somaris/7 Syngo CT 2011A was used to assess the images and to obtain the total volumes of both sinuses and grafts. The volume calculation method for the sequential images was the sum of the areas. This method requires the manual delimitation of graft perimeter, using a mouse, on each of the image slices, in its full extension. The individual volume of each slice is added to the volume of the previous sections. When the total volume of sinuses and grafts is fully marked on the sequential images, the volumetric function of the software is triggered and the final result automatically equals the graft volume (Jonhansson et al. 2001, Cosso et al. 2013). This procedure was performed by an experienced radiologist, trained and calibrated with a Kappa (k) index of 0.79. For each slice, the software calculates the volume within the identified area of interest in cm3, taking into consideration the thickness of the slice. These procedures were performed for all examinations from the first measurement of
Material and methods Study design
The Ethics and Research Committee of PUCMINAS approved this research under ID number 037683/2012, characterized as an analytical, longitudinal and cohort study. A multislice computerized tomography was performed before, 15 days and 180 days after graft sinus lift surgery, in patients who were candidates for implant rehabilitation treatment in the posterior maxilla. The factor studied was the influence of overall maxillary sinus volume (T0) on post-surgical graft dimensional changes after 180 days (T2). One hundred and fifty tomographic examinations, from 43 individuals subjected to maxillary sinus lifting with a total number of 50 sinuses, were used for this study. Maxillary
Chart 1. Literature comparison of the average volumetric dimensional changes Year
Author
Exam
Material
Sample
TF
DC-T2
DC-TF
2006 2008
Wanschitz et al. Kirmeier et al.
PR– CT CT
(33 SM) (25 SM)
14 D 14 D
4–11 M 6M
– –
13.9% 26.0%
– –
2012
Klijn et al.
CBCT
(38 SM)
14 D
5M
–
Arasawa et al. Umanjec-Korac et al.
CT CBCT
(11 SM) (29 SM)
3M 4–6 M
23 M 24 M
– –
2013
Kim et al.
CBCT
(14 SM)
6M
12 M
–
2013
Sbordone et al.
CT
(23 SM)
0–12 M
13–24 M
25.0% 25.0% 24.8% 19.98% 17.37% 37.6% 41.2% –
–
2012 2013
PAB Algiporeâ PAB Algiporeâ DBB PAB ABB PAB PAB/DBB DBB DBB PHB ABB PAB
T1
T2
61–72 M
– – – 21.5% 39.2%
PAB, particulate autogenous bone; ABB, autogenous bone block; PHB, particulate homologous bone; DBB, Bio-Ossâ; CT, 3D computerized tomography; CBCT, cone beam computerized tomography; PR, panoramic radiographic; SM, maxillary sinus; D, days; M, months; T1; T2 and TF, post-operative times; DC-T2 and DC-TF, dimensional changes shrinkage percentage in periods. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
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Favato et al Maxillary sinus volume and graft changes
Statistical analysis
Statistical analysis was based on Student’s t-test using linear regression and Pearson’s correlation, regardless of age or gender. Dependent variables were initial total maxillary sinus average volume (T0) vs. average dimensional changes of the graft (T2-T1). The level of significance of the tests was set at 5%.
(a)
(b)
Results
(c) Fig. 1. Sinus volume delimitation done using Syngo CT 2011 A Volume slices. Axial–Sagital–Coronal view.
(a)
(b)
(c)
Fig. 2. Graft delimitation in T1 done using Syngo CT 2011 A Volume slices. (a) Axial view; (b) Sagital view; (c) Coronal view.
(a)
(b)
(c)
Fig. 3. Graft delimitation in T2 one using Syngo CT 2011 A Volume slices. (a) Axial view; (b) Sagital view; (c) Coronal view.
maxillary sinus volume (T0) (Fig. 1) and graft volume after 15 days post-op (T1) (Fig. 2) and were reassessed at a second moment (T2) (Fig. 3), graft volume after 180 days (Jonhansson et al. 2001). Based on this tomographic image assessment method, the following items were measured: initial total volume of sinus, initial
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volume of graft material (15 days)and bone graft volume after a 180-day healing period. Using these measurements, the calculations of graft dimensional changes between the two time intervals, the correlation between total sinus volumes and degree of dimensional changes, in relation to the different grafting materials used in the study, were performed.
The data obtained from the sample (50 sinuses) were assessed to test the correlation between graft contraction and the maxillary sinus volume (Table 1). Once the volumes of the maxillary sinuses were measured, a cutoff value was established to determine a limit reference value (15.2 cm3). Sinuses greater than 15.2 cm3 in volume were considered large, and ones smaller than that were considered small. The average volume found for the maxillary sinuses of the sample was 15.65 cm3 (r 3.44 cm3), and the average percentage for graft contraction was 19.28% (r 14%). In this way, the minimum maxillary total sinus volume assessed in the sample was 7.03 cm3 and the maximum maxillary total sinus volume measured was 23.85 cm3. Figure 4 shows sinus volume dispersion vs. the contraction logarithm. Endobonâ is represented by the green line, with the lower contraction average (8.04%), while other biomaterials present higher contraction rates. The inclination of the arrow represents the correlation between the sinus volume and the graft dimensional changes. As it is virtually parallel to the horizontal axis, at an angle that is not considered statistically different from zero, this correlation is not significant at the 5% significance level. A t-test was also performed to check the Pearson’s correlation coefficient between the variables graft contraction and sinus volume (Table 2). Once again, the P-value is higher than the 5% significance level, and the null hypothesis cannot be rejected for any of the cases. The patients were divided into two groups. The cutoff was made based on the total sinus volume, according to the median. Those volumes greater than 15.74 mm³ were assigned to group 2 and group 1, each sinus volume was less than the median. Each group contained 25 patients. Table 3 summarizes this distribution and the means of the graft contractions observed for each of the graft materials.
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Favato et al Maxillary sinus volume and graft changes
Table 1. Sample summary statistics Graft material
N sinuses
N sinuses > 15.2 cm³
Sinus volume (cm³)
Graft volume 15 days (cm³)
Graft volume 180 days (cm³)
Graft shrinkage (cm³)
Graft shrinkage (%)
Bone Ceramic
12
11
Bone Ceramic + Emdogain
10
2
Endobon
17
12
Fresh frozen allogenic particulated bone Total general
11
10
50
35
15.88 (0.90) 13.65 (5.00) 16.94 (4.13) 15.23 (0.24) 15.65 (3.44)
1.68 (0.29) 1.74 (0.57) 1.60 (0.44) 1.63 (0.39) 1.65 (0.42)
1.35 (0.32) 1.34 (0.46) 1.46 (0.35) 1.06 (0.27) 1.32 (0.37)
0.33 (0.17) 0.39 (0.24) 0.14 (0.13) 0.57 (0.32) 0.33 (0.26)
20.28% (0.10) 21.83% (0.09) 8.04% (0.05) 33.24% (0.16) 19.28% (0.14)
Sinus volume x Graft contraction 0
ln(Graft contraction)
–0.5 –1 –1.5 –2 –2.5 –3 –3.5 7
5
9
11
13
17
15
19
21
23
25
Sinus volume (cm³) BoneCeramic BoneCeramicEmdogain
Fresh frozen allogenic particulated bone
BoneCeramic (Y = –1.367 + 0.02X)
Endobon (Y = –2.587 + 0.02X)
BoneCeramicEmdogain (Y = –1.539 + 0.02X)
Fresh frozen allogenic particulated bone (Y = –1.120 + 0.02X)
Fig. 4. Sinus volume 9 Graft contraction.
Table 2. Pearson’s correlation coefficient – correlation [sinus volume 3 graft material shrinkage]
Correlation T statistics Freedom degrees Bilateral P-value
Bone Ceramic + Emdogain
Bone ceramic
0.004 0.010 8 0.992
0.163 0.522 10 0.613
Discussion Up to the time of this study, there had been no studies reporting results that could deter-
Endobon
Fresh frozen allogenic particulated bone
Total
0.214 0.849 15 0.409
0.448 1.503 9 0.167
0.112 0.778 48 0.44
mine the influence of the three-dimensional shape of the palatal and buccal walls on bone graft healing over the graft placed between these walls. It is also worth considering
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
whether a graft placed in a narrow sinus can heal and mineralize rapidly and successfully, when compared to a graft placed in a larger and more extensive sinus (Soardi et al. 2011). In the present study, the total volume of the 50 maxillary sinus over the grafting materials, fresh frozen allogenic particulated bone (Marilia Bone Bankâ), hydroxyapatite (Endobonâ), hydroxyapatite + beta-tricalcium phosphate (Bone Ceramicâ) and Bone Ceramicâ + Emdogainâ, revealed no statistical significance.
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Favato et al Maxillary sinus volume and graft changes
Table 3. Summarizes the graft contractions observed for each group according to the median cutoff point established
Material
15 mm as being large and sizes ≤ 15 mm as being small. In the present study, the maxillary total sinus volume was measured in cm3 and used as a reference. The average maxillary sinus volume found for
this sample was 15.65 cm3 (r 3.44 cm3), and the average dimensional change percentage of grafts was 19.28% (r 14%). Conversely, the present study has some limitations, as the type of graft materials as well as the heterogeneity of the maxillary sinus volume could influence the tendency of the results. In this context, when comparing the correlation of the maxillary total sinus volume with the dimensional changes that occurred using different grafting materials, the present study contradicts the hypothesis that extensive sinus cavities influence graft stability (Kolerman et al. 2008; Soardi et al. 2011).
Conclusion The present study did not reveal evidence that maxillary overall sinus volume has an impact on the graft dimensional changes. Further studies in other populations and with different grafts are needed as, up to the present moment, there is no research that applies the proposed methodology.
Acknowledgements: The author Elton G. Zen obio was supported by the Post Doctoral Senior Program, PDS 151009/20120-CNPQ and FAPEMIG program: CDS – APQ-01354-11, Brazil.
Conflict of interest and source of funding statement The authors declare no conflict of interest related to this study.
References Abubaker, A.O. (1999) Applied anatomy of maxillary sinus. Oral Maxillofacial Surgery Clinical of North America 11: 1–13. Arasawa, M., Oda, Y., Kobayashi, T., Uoshima, K., Nishiyama, H., Hoshina, H. & Saito, C. (2012) Evaluation of bone volume changes after sinus floor augmentation with autogenous bone grafts. International Journal Oral Maxillofacial Surgery 41: 853–857. Blanton, P. & Biggs, N. (1969) Eighteen hundreds of controversy: the paranasal sinuses. American Journal Anatomic 124: 135–148. Block, M.S., Kent, J.N., Kallukaran, F.U., Thumthy, K. & Weinberg, R. (1998) Bone maintenance 5 to 10 years after sinus grafting. Journal Oral & Maxillofacial Implants 56: 706–714. Cosso, M.G., Brito, R.B., Jr, Piattelli, A., Shibli, J.A. & Zen obio, E.G. (2013) Volumetric dimensional
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change of autogenous bone and the mixture of hydroxyapatite and autogenous bone graft, in human maxillary sinus augmentation. A multislice tomographic study. Clinical Oral Implants Research. doi: 10.1111/clr.12261xt. Emtiaz, S., Caram^es, J.M.M. & Pragosa, A. (2006) An alternative sinus floor elevation procedure: trephine osteotomy. Implant Dentistry 15: 171–177. Geurs, N., Wang, I.C., Shulman, L.B. & Jeffcoat, M.K. (2001) Retrospective radiographic analysis of sinus graft and implant placement procedures from the Academy of Osteointegration Consensus Conference on sinus graft. The International Journal of Periodontics and Restorative Dentistry 21: 517–523. Gray, C.F., Redpath, T.W., Bainton, R. & Smith, F.W. (2001) Magnetic resonance imaging assessment of a sinus lift operation using re-oxi-
dised cellulose (Surgicels) as graft material. Clinical Oral Implants Research 12: 526–530. Jensen, O.T. & Greer, R. (1992) Immediate placing of osseointegrated implants into the maxillary sinus augmented with mineralized cancellous allograft and Gore Tex: second stage surgical and histological findings. In: Laney, W.R. & Tolman, D.E., eds. Tissue Integration. Oral Orthopaedic and Maxillofacial Reconstruction, 321–333. Chicago: Quintessence. Jensen, J., Kragskov, J., Wenzel, A. & SinddetPedersen, S. (1997) Volumetric of bone grafts by three-dimensional computed tomographic reconstructions: an animal study in the mini-pig. Dento Maxillofacial Radiology 27: 41–44. Jonhansson, B., Grepe, A., Wannfors, K., Aberg, P. & Hirsch, J.M. (2001) Volumetric of simulated bone grafts in edentulous maxilla by computed
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tomography: an experimental study. Dento Maxillofacial Radiology 30: 153–156. Kim, E.S., Moon, S.Y., Kim, S.G., Park, H.C. & Oh, J.S. (2013) Three-dimensional volumetric analysis after sinus grafts. Implant Dentistry 22: 170–174. Kirmeier, R., Payer, M., Wehrschuetz, M., Jakse, N., Platzer, S. & Lorenzoni, M. (2008) Evaluation of three-dimensional changes after sinus floor augmentation with different grafting materials. Clinical Oral Implants Research 19: 366–372. Klijn, R.J., Beucken, J.J.P.V.D., Bronkhorst, E.M., Berge, S.J., Meijer, G.J. & Jansen, J.A. (2012) Predictive value of ridge dimensions on autologous bone graft resorption in staged maxillary sinus augmentation surgery using Cone-Beam CT. Clinical Oral Implants Research 23: 409–415. Kolerman, R., Tal, H. & Moses, O. (2008) Histomorphometric analysis of newly formed bone after maxillary sinus floor augmentation using ground cortical bone allograft and internal collagen membrane. Journal Periodontology 79: 2104– 2111. Mardinger, O., Nissan, J. & Chaushu, G. (2007) Sinus floor augmentation with simultaneous implant placement in the severely atrophic maxilla: technical problems and complications. Journal Periodontology 78: 1872–1877. Maresh, M.M. (1940) Paranasal sinuses from birth to late adolescence: size of the paranasal sinuses as observed in routine posterior-anterior roentgen-
ograms. American Journal Diseases Children 60: 55–78. Misch, C.E. (2008) Maxillary sinus anatomy, pathology and graft surgery. In: Misch, C.E., ed. Contemporary Implant Dentistry, 3rd edition, 914–915. St. Louis, MO: Mosby. Nystr€ om, E., Ahlqvist, J., Kahnberg, K.E. & Rosenquist, J.B. (1996) Autogenous onlay bone grafts fixed with screw implants for the treatment of severely resorbed maxillae. International Journal Oral Maxillofacial Implants 25: 351–359. Peleg, M., Garg, A.K. & Mazor, Z. (2006) Predictability of simultaneous implant placement in the severely atrophic posterior maxilla: a 9-year longitudinal experience study of 2.132 implants placed into 731 human sinus grafts. International Journal Oral Maxillofacial Implants 21: 94–102. Pjetursson, B.E., Tan, W.C., Zwahlen, M. & Lang, N.P. (2008) A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation. Journal Clinical Periodontology 35: 216– 240. Rios, H., Avila, G., Galindo, P., Bratu, E. & Wang, H.L. (2009) The influence of remaining alveolar bone upon lateral window sinus augmentation implants survival. Implant Dentistry 18: 402–412. Sbordone, C., Totim, P., Guidetti, F., Califano, L., Bufo, P. & Sbordone, L. (2013) Volume changes of autogenous bone after sinus lifting and grafting procedures: a 6-year computerized tomographic
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follow-up. Journal CranioMaxilloFacial Surgery 41: 235–241. Similer, D.G., Johnson, P.W., Lozada, J.L., Misch, C.E., Rosenlicht, J.L., Tatum, O.H. & Wagner, J.R. (1992) Sinus lift grafts and endosseous implants. Dental Clinics of North America 36: 151–186. Soardi, C.M., Spinato, S., Zaffe, D. & Wang, H.L. (2011) Atrophic maxillary floor augmentation by mineralized human bone allograft in sinuses of different size: a histologic and histomorphometric analysis. Clinical Oral Implants Research 22: 560–566. Uchida, Y., Goto, M., Katsuki, T. & Soejima, Y. (1998) Measurement of maxillary sinus volume using computerized tomographic images. International Journal Oral Maxillofacial Implants 13: 811–818. Umanjec-Korac, S., Wu, G., Hassan, B., Liu, Y. & Wismeijer, D. (2013) A retrospective analysis of the resorption rate of deproteinized bovine bone as maxillary sinus graft material on cone beam computed tomography. Clinical Oral Implants Research. doi: 10.1111/clr.12174. Wanschitz, F., Figl, M., Wagner, A. & Rolf, E. (2006) Measurement of volume changes after sinus floor augmentation with a phycogenic hydroxyapatite. International Journal Oral Maxillofacial Implants 21: 433–438. Zinner, I.D. & Small, S.A. (1996) Sinus-lift graft: using the maxillary sinuses to support implants. Journal American Dental Association 127: 51–57.
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Clin. Oral Impl. Res. 26, 2015 / 1450–1455
Impact of human maxillary sinus volume on grafts dimensional changes used in maxillary sinus augmentation: a multislice tomographic study
Authors’ affiliations: M ario N. Favato, Maurıcio G. Cosso, Elton G. Zen obio, Department of Dentistry, Implant Master Program, PUCMINAS, Belo Horizonte, Brazil Bruno C.L. Vidigal, Fl avio R. Manzi, Department of Dentistry, Radiology Master Program, PUCMINAS, Belo Horizonte, Brazil Jamil A. Shibli, Department of Periodontology and Oral Implantology, UNG, Guarulhos, Brazil
Key words: Sinus lift, Bone formation, Sinus volume, Biomaterial, Multislice tomography
Corresponding author: Elton Goncßalves Zen obio Department of Dentistry Implant Master Program Av. Dom Jos e Gaspar – 500, 46 Hall CEP – 30535.610, Belo Horizonte, Brazil. Tel.: +55 31 33194414 Fax: +553133194410 e-mail: [email protected]
Abstract Purpose: To assess the influence of complete maxillary sinus volume on the dimensional changes of different grafts used in maxillary sinus lift. Materials and Methods: Analysis of 50 surgical procedures of maxillary sinus lift performed on 43 subjects using different grafting materials: fresh frozen allogenic particulated bone (11), hydroxyapatite (Endobonâ) (17), 60% hydroxyapatite + 40% beta-tricalcium phosphate (Bone Ceramicâ) (12) and Bone Ceramicâ + Emdogainâ (10). One hundred and fifty multislice tomographic images of the maxillary sinus were obtained using the software Syngo CT 2011 A VOLUME, measuring complete maxillary sinus volume (T0) and dimensional changes of different graft materials during periods of 15 days (T1) and 180 days (T2). The factor studied was the influence of maxillary sinus volume on the dimensional changes of different graft materials used in maxillary sinus lift in patients with posterior edentulism. Data obtained were assessed using the Student’s t-test and Pearson’s correlation coefficient. Results: No correlation (r 0.112) between the total maxillary sinus volume and the dimensional changes of the different graft materials used in this study was observed (P > 0.05). Conclusion: This study demonstrated that there is no sufficient evidence to support the thesis that the volume of the maxillary sinus influences the contraction of the grafts, at least on sample or the biomaterials evaluated in this cohort study.
Date: Accepted 27 August 2014 To cite this article: Favato MN, Vidigal BCL, Cosso MG, Manzi FR, Shibli JA, Zen obio EG. Impact of human maxillary sinus volume on grafts dimensional changes used in maxillary sinus augmentation: a multislice tomographic study. Clin. Oral Impl. Res. 26, 2015, 1450–1455 doi: 10.1111/clr.12488
1450
The maxillary sinus is the largest of all paranasal sinuses: pyramidal shaped, with approximate dimensions of 20 mm length, 40 mm height and 30 mm depth (Emtiaz et al. 2006). Authors have suggested some hypotheses about the functions of the maxillary sinus (Blanton & Biggs 1969): moistening inspired air; expanding the area of the olfactory membrane; absorbing direct impact to the skull structure; secreting mucus to humidify the nasal cavity; insulating the brain thermally; contributing to facial growth; and decreasing the weight of the skull. At six years of age, the cavity starts to take the pyramidal shape and becomes radiographically visible. Maxillary sinus volume has a fast growth rate in children up to 12 years of age, after which its growth rate decreases and becomes stable after the eruption of the last molars (Maresh 1940; Abubaker 1999).
Dental loss induces maxillary sinus expansion, possibly creating a union between the sinus floor and the crest of the remaining alveolar ridge (Misch 2008). This expansion is related to sinus height and length, rather than depth (Uchida et al. 1998). After tooth extraction, a 25% decrease is observed in ridge volume during the first year, reaching 40–60% in length during the first three years (Misch 2008). Lateral access sinus augmentation technique has been widely studied and described as a safe and highly predictable treatment (Similer et al. 1992; Zinner & Small 1996; Block et al. 1998; Pjetursson et al. 2008). To assess bone-grafting procedures in maxillofacial reconstructive surgeries, it is important to have reliable and accurate diagnostic methods, capable of determining the longitudinal survival of bone grafts. In this context,
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Favato et al Maxillary sinus volume and graft changes
three-dimensional computerized tomography (3D CT scan) assesses the correlation between the real volume measurements of bone grafts and the volumes measured by the 3D CT scan, to determine the accuracy of this type of examination (Jensen et al. 1997). Uchida et al. (1998) determined the maxillary sinus volume and took it as a reference to define the volume of bone graft needed to allow further implant placement. Taking into account the individual differences in terms of maxillary sinus volume and the resorption of grafted materials, an approximate volume of 5.46 cm3 was needed for a 15-mm lift and approximately 7.96 cm3 for a 20-mm lift. Studies report results regarding the volumetric stability of different materials used in maxillary sinus lift for further osseointegrated implant placement (Chart 1). It has been reported that the higher the residual bone, the greater the success rate, regardless of whether one- or two-stage approaches were used (Jensen & Greer 1992; Geurs et al. 2001; Peleg et al. 2006; Mardinger et al. 2007; Rios et al. 2009). The low percentage of new bone formation in three patients (17%) can be partly explained by the presence of very extensive nasal cavities, either in the mesial–distal or buccal–palatal directions. Larger maxillary sinuses may present reduced osteogenic potential as a result of the distance between the source of osteogenic cells and the peripheral angiogenesis. Therefore, from the biological standpoint, they merely assumed that the larger volume of maxillary sinus determines a greater graft contraction and a longer new bone formation time (Kolerman et al.2008). Soardi et al. (2011), in human histological assessments of mineralized bone graft to maxillary sinus floor elevation (ridge height 15 mm. Results of this study demonstrated that of the 15 sinuses classified as large, two required a longer maturation period to attain an adequate amount of newly formed bone. Despite the different studies about the volumetric stability of different grafting materials for sinus floor lifting procedures (Wanschitz et al. 2006; Kirmeier et al. 2008; Arasawa et al. 2012; Klijn et al. 2012; Cosso et al. 2013; Kim et al. 2013; Sbordone et al. 2013; Umanjec-Korac et al. 2013) none of them has assessed the influence of the total volume of the sinus in the shrinkage of grafted materials. Perhaps, these theories (Gray et al. 2001; Jonhansson et al. 2001), about the relationship of the influence of the graft volume dimensional changes, materials characteristics and the total volume of maxillary sinus have not yet been clarified.
Images analysis
A 128 multislice tomography was used to capture the images (Somatom, Siemens, Erlangen, Germany). Multislice tomographic images were used to assess the mass volume of the sinus lift grafts as a way to measure the degree of volume alteration between the two healing stages. The software Siemens SOMATOM, Somaris/7 Syngo CT 2011A was used to assess the images and to obtain the total volumes of both sinuses and grafts. The volume calculation method for the sequential images was the sum of the areas. This method requires the manual delimitation of graft perimeter, using a mouse, on each of the image slices, in its full extension. The individual volume of each slice is added to the volume of the previous sections. When the total volume of sinuses and grafts is fully marked on the sequential images, the volumetric function of the software is triggered and the final result automatically equals the graft volume (Jonhansson et al. 2001, Cosso et al. 2013). This procedure was performed by an experienced radiologist, trained and calibrated with a Kappa (k) index of 0.79. For each slice, the software calculates the volume within the identified area of interest in cm3, taking into consideration the thickness of the slice. These procedures were performed for all examinations from the first measurement of
Material and methods Study design
The Ethics and Research Committee of PUCMINAS approved this research under ID number 037683/2012, characterized as an analytical, longitudinal and cohort study. A multislice computerized tomography was performed before, 15 days and 180 days after graft sinus lift surgery, in patients who were candidates for implant rehabilitation treatment in the posterior maxilla. The factor studied was the influence of overall maxillary sinus volume (T0) on post-surgical graft dimensional changes after 180 days (T2). One hundred and fifty tomographic examinations, from 43 individuals subjected to maxillary sinus lifting with a total number of 50 sinuses, were used for this study. Maxillary
Chart 1. Literature comparison of the average volumetric dimensional changes Year
Author
Exam
Material
Sample
TF
DC-T2
DC-TF
2006 2008
Wanschitz et al. Kirmeier et al.
PR– CT CT
(33 SM) (25 SM)
14 D 14 D
4–11 M 6M
– –
13.9% 26.0%
– –
2012
Klijn et al.
CBCT
(38 SM)
14 D
5M
–
Arasawa et al. Umanjec-Korac et al.
CT CBCT
(11 SM) (29 SM)
3M 4–6 M
23 M 24 M
– –
2013
Kim et al.
CBCT
(14 SM)
6M
12 M
–
2013
Sbordone et al.
CT
(23 SM)
0–12 M
13–24 M
25.0% 25.0% 24.8% 19.98% 17.37% 37.6% 41.2% –
–
2012 2013
PAB Algiporeâ PAB Algiporeâ DBB PAB ABB PAB PAB/DBB DBB DBB PHB ABB PAB
T1
T2
61–72 M
– – – 21.5% 39.2%
PAB, particulate autogenous bone; ABB, autogenous bone block; PHB, particulate homologous bone; DBB, Bio-Ossâ; CT, 3D computerized tomography; CBCT, cone beam computerized tomography; PR, panoramic radiographic; SM, maxillary sinus; D, days; M, months; T1; T2 and TF, post-operative times; DC-T2 and DC-TF, dimensional changes shrinkage percentage in periods. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
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Favato et al Maxillary sinus volume and graft changes
Statistical analysis
Statistical analysis was based on Student’s t-test using linear regression and Pearson’s correlation, regardless of age or gender. Dependent variables were initial total maxillary sinus average volume (T0) vs. average dimensional changes of the graft (T2-T1). The level of significance of the tests was set at 5%.
(a)
(b)
Results
(c) Fig. 1. Sinus volume delimitation done using Syngo CT 2011 A Volume slices. Axial–Sagital–Coronal view.
(a)
(b)
(c)
Fig. 2. Graft delimitation in T1 done using Syngo CT 2011 A Volume slices. (a) Axial view; (b) Sagital view; (c) Coronal view.
(a)
(b)
(c)
Fig. 3. Graft delimitation in T2 one using Syngo CT 2011 A Volume slices. (a) Axial view; (b) Sagital view; (c) Coronal view.
maxillary sinus volume (T0) (Fig. 1) and graft volume after 15 days post-op (T1) (Fig. 2) and were reassessed at a second moment (T2) (Fig. 3), graft volume after 180 days (Jonhansson et al. 2001). Based on this tomographic image assessment method, the following items were measured: initial total volume of sinus, initial
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volume of graft material (15 days)and bone graft volume after a 180-day healing period. Using these measurements, the calculations of graft dimensional changes between the two time intervals, the correlation between total sinus volumes and degree of dimensional changes, in relation to the different grafting materials used in the study, were performed.
The data obtained from the sample (50 sinuses) were assessed to test the correlation between graft contraction and the maxillary sinus volume (Table 1). Once the volumes of the maxillary sinuses were measured, a cutoff value was established to determine a limit reference value (15.2 cm3). Sinuses greater than 15.2 cm3 in volume were considered large, and ones smaller than that were considered small. The average volume found for the maxillary sinuses of the sample was 15.65 cm3 (r 3.44 cm3), and the average percentage for graft contraction was 19.28% (r 14%). In this way, the minimum maxillary total sinus volume assessed in the sample was 7.03 cm3 and the maximum maxillary total sinus volume measured was 23.85 cm3. Figure 4 shows sinus volume dispersion vs. the contraction logarithm. Endobonâ is represented by the green line, with the lower contraction average (8.04%), while other biomaterials present higher contraction rates. The inclination of the arrow represents the correlation between the sinus volume and the graft dimensional changes. As it is virtually parallel to the horizontal axis, at an angle that is not considered statistically different from zero, this correlation is not significant at the 5% significance level. A t-test was also performed to check the Pearson’s correlation coefficient between the variables graft contraction and sinus volume (Table 2). Once again, the P-value is higher than the 5% significance level, and the null hypothesis cannot be rejected for any of the cases. The patients were divided into two groups. The cutoff was made based on the total sinus volume, according to the median. Those volumes greater than 15.74 mm³ were assigned to group 2 and group 1, each sinus volume was less than the median. Each group contained 25 patients. Table 3 summarizes this distribution and the means of the graft contractions observed for each of the graft materials.
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Favato et al Maxillary sinus volume and graft changes
Table 1. Sample summary statistics Graft material
N sinuses
N sinuses > 15.2 cm³
Sinus volume (cm³)
Graft volume 15 days (cm³)
Graft volume 180 days (cm³)
Graft shrinkage (cm³)
Graft shrinkage (%)
Bone Ceramic
12
11
Bone Ceramic + Emdogain
10
2
Endobon
17
12
Fresh frozen allogenic particulated bone Total general
11
10
50
35
15.88 (0.90) 13.65 (5.00) 16.94 (4.13) 15.23 (0.24) 15.65 (3.44)
1.68 (0.29) 1.74 (0.57) 1.60 (0.44) 1.63 (0.39) 1.65 (0.42)
1.35 (0.32) 1.34 (0.46) 1.46 (0.35) 1.06 (0.27) 1.32 (0.37)
0.33 (0.17) 0.39 (0.24) 0.14 (0.13) 0.57 (0.32) 0.33 (0.26)
20.28% (0.10) 21.83% (0.09) 8.04% (0.05) 33.24% (0.16) 19.28% (0.14)
Sinus volume x Graft contraction 0
ln(Graft contraction)
–0.5 –1 –1.5 –2 –2.5 –3 –3.5 7
5
9
11
13
17
15
19
21
23
25
Sinus volume (cm³) BoneCeramic BoneCeramicEmdogain
Fresh frozen allogenic particulated bone
BoneCeramic (Y = –1.367 + 0.02X)
Endobon (Y = –2.587 + 0.02X)
BoneCeramicEmdogain (Y = –1.539 + 0.02X)
Fresh frozen allogenic particulated bone (Y = –1.120 + 0.02X)
Fig. 4. Sinus volume 9 Graft contraction.
Table 2. Pearson’s correlation coefficient – correlation [sinus volume 3 graft material shrinkage]
Correlation T statistics Freedom degrees Bilateral P-value
Bone Ceramic + Emdogain
Bone ceramic
0.004 0.010 8 0.992
0.163 0.522 10 0.613
Discussion Up to the time of this study, there had been no studies reporting results that could deter-
Endobon
Fresh frozen allogenic particulated bone
Total
0.214 0.849 15 0.409
0.448 1.503 9 0.167
0.112 0.778 48 0.44
mine the influence of the three-dimensional shape of the palatal and buccal walls on bone graft healing over the graft placed between these walls. It is also worth considering
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
whether a graft placed in a narrow sinus can heal and mineralize rapidly and successfully, when compared to a graft placed in a larger and more extensive sinus (Soardi et al. 2011). In the present study, the total volume of the 50 maxillary sinus over the grafting materials, fresh frozen allogenic particulated bone (Marilia Bone Bankâ), hydroxyapatite (Endobonâ), hydroxyapatite + beta-tricalcium phosphate (Bone Ceramicâ) and Bone Ceramicâ + Emdogainâ, revealed no statistical significance.
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Favato et al Maxillary sinus volume and graft changes
Table 3. Summarizes the graft contractions observed for each group according to the median cutoff point established
Material
15 mm as being large and sizes ≤ 15 mm as being small. In the present study, the maxillary total sinus volume was measured in cm3 and used as a reference. The average maxillary sinus volume found for
this sample was 15.65 cm3 (r 3.44 cm3), and the average dimensional change percentage of grafts was 19.28% (r 14%). Conversely, the present study has some limitations, as the type of graft materials as well as the heterogeneity of the maxillary sinus volume could influence the tendency of the results. In this context, when comparing the correlation of the maxillary total sinus volume with the dimensional changes that occurred using different grafting materials, the present study contradicts the hypothesis that extensive sinus cavities influence graft stability (Kolerman et al. 2008; Soardi et al. 2011).
Conclusion The present study did not reveal evidence that maxillary overall sinus volume has an impact on the graft dimensional changes. Further studies in other populations and with different grafts are needed as, up to the present moment, there is no research that applies the proposed methodology.
Acknowledgements: The author Elton G. Zen obio was supported by the Post Doctoral Senior Program, PDS 151009/20120-CNPQ and FAPEMIG program: CDS – APQ-01354-11, Brazil.
Conflict of interest and source of funding statement The authors declare no conflict of interest related to this study.
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