ORIGINAL ARTICLE

One-Year Volume Stability of Human Facial Defects Filled With a A-Tricalcium PhosphateYHydroxyl Apatite Mixture (Atlantik) Gerhard Koendert Pieter Bittermann, MD,* Nard G. Janssen, MD, DMD,* Maarten van Leeuwen, MD,Þ and Robert J. J. van Es, MD, DMD* Introduction: We investigated the applicability and 1-year stability of a A-tricalcium phosphateYhydroxyl apatite mixture (Atlantik) for secondary reconstruction of craniofacial defects and the application of OsiriX in evaluating bone and implant volumes. Methods: We included 6 patients (25Y59 years) with craniofacial defects. A computed tomography scan was made preoperative, directly postoperative, and at least 1 year postoperative to evaluate volume changes. OsiriX was used to quantify volumes of the implanted Atlantik. Measurements were performed by 2 independent investigators and analyzed by calculating both Pearson correlation and interclass correlation coefficient. Results: After 1 year, the mean volume reduction of the implanted Atlantik was 9.8%. The absolute volume reduction in 1 year was 0.38 cm3 (range, 0.10Y0.69 cm3). Pearson correlation test was 0.996, with a significance level of P G 0.01, and the interclass correlation coefficient was 0.998. Conclusions: Atlantik is a stable osteoconductive material for the repair of various craniofacial defects. There is a reduction of only 10% of the augmented volume in the long term. Applying OsiriX for computed tomography image volume analysis proved to be a wellreproducible technique. Key Words: Craniofacial defects, bTCP, hydroxyl apatite, reconstruction, volume, stability (J Craniofac Surg 2014;25: 372Y374)

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or the repair of craniofacial defects, several materials can be used, such as autologous or allograft bone, metals, bioceramics, plastics, and composites.1,2 The ideal biomaterial for the reconstruction of three-dimensional facial defects has to be an easy-to-handle synthetic bone substitute, which has volume stability, that is, nonresorbing, and induces bone ingrowth.3 This is especially wanted in secondary augmentation of orbital floor defects to keep the globe in position and resurfacing of facial bones to maintain facial bony contours. Osteoconductive ceramics are used increasingly worldwide, and literature shows their easy applicability and low infection rate.4 The ceramic A-tricalcium phosphate (bTCP) conducts bone ingrowth, and is completely resorbed by the human body. Hydroxyl apatite (HA) is a bone substitute that is hardly resorbed. However, bone ingrowth between HA granules is dependent on its surface structure and sometimes minimal.5Y7 Therefore, a mixture of bTCP and HA seems ideal as HA will contribute to the stability of volume and shape, whereas bTCP will accommodate the osteoconduction In vitro research showed that an HA:bTCP ratio of 3:1 was found optimal in inducing bone ingrowth without being resorbed, resulting in a stable osteoconductive material.8 Atlantik has an HA:bTCP ratio of 7:3, which makes it an ideal bone substitute for secondary reconstruction in maxillofacial practice as the applied volume has to be stable over time. Atlantik is packed as small grains, which makes it easy to apply in bony defects and create tailor-made adjustments during surgery. However, the applicability and long-term properties of Atlantik in clinical practice have not been investigated yet. In the following study, its in vivo volume stability and bone ingrowth are evaluated. In this study, we also evaluated the applicability of the DICOM viewer OsiriX for measuring the volumes of implanted Atlantik. This is a widely used open-source DICOM viewer that has been used in the past for calculating three-dimensional alveolar cleft defects.9

MATERIALS AND METHODS Patients

From the Departments of *Oral and Maxillofacial Surgery and †Radiology, University Medical Center Utrecht, the Netherlands. Received October 29, 2013. Accepted for publication December 2, 2013. Address correspondence and reprint requests to Gerhard Koendert Pieter Bittermann, MD, Department of Oral and Maxillofacial Surgery University Medical Center Utrecht NL, Heidelberglaan 100, 3584 CX Utrecht, the Netherlands; E-mail: [email protected] No financial support was received for this study. The authors report no conflicts of interest. Copyright * 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000000636

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Six consecutive patients with secondary facial bony defects (4 orbital floor, 1 frontal, and 1 temporal bone) aged between 25 and 59 years were reconstructed using Atlantik and followed up at the Department of Maxillofacial Surgery, University Medical Centre Utrecht. All patients underwent multislice computed tomography (CT) preoperatively, directly postoperatively, and at least 1 year postoperatively.

Atlantik Atlantik (Medical Biomat, Vaulx en Velin, France) is mixture of HA and bTCP with an HA:bTCP ratio of 7:3. It is available as microporous and macroporous granules (macropores: 0.5 mm) in volumes of 1 mL.

The Journal of Craniofacial Surgery

& Volume 25, Number 2, March 2014

Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.

The Journal of Craniofacial Surgery

Facial Defects Filled With A-TCP-HA

& Volume 25, Number 2, March 2014

Figure 2. Three-dimensional volume calculated by combining the regions of interest. Figure 1. Placement of regions of interest.

Surgical Procedure Preoperatively, a multislice CT scan was performed to evaluate the defect. The radiologist calculated the volume of the defect, to estimate the amount of Atlantik needed for the procedure. To calculate the amount of Atlantik necessary for reconstruction of the orbital floor, the volume of the intact orbit was subtracted from the defective side. The difference dictated the volume needed for reconstruction. A suitable orbital floor was a prerequisite to use this technique. All patients were treated by the same surgeon. During surgery, the bony defect was located and exposed. Atlantik was mixed in a 2- or 5-mL plastic syringe with a minimum of fibrin glue (Tissuecol) to make it easier to handle and then placed into the defect.5

Imaging After surgery, a first postoperative CT scan was made within 3 months’ time, to evaluate the position of the material. At least 1 year postoperatively, another CT scan was made for evaluation of the reconstruction and to see if the implanted material was still in position.10

Data Analysis The data of the CT images were analyzed with OsiriX DICOM viewer (Pixmeo; Apple Inc, Geneva, Switzerland)9 (Figs. 1 and 2). To ensure the reproducibility of the measurements, 2 independent investigators analyzed the images and calculated the volume of the implanted Atlantik. OsiriX was used to calculate the volume of the augmented material in both postoperative CT images.

Statistical analysis Statistical analyses were performed by SPSS 20 IBM (Statistical Package for the Social Sciences; SPSS Inc, Chicago, IL). Volume reduction and mean volume reduction were calculated. Because the relation was linear, measured volume differences by both investigators

were calculated using both a Pearson correlation and the interclass correlation coefficient (ICC).6 A good interinvestigator correlation exists if the ICC is more than 0.7.

RESULTS The population consisted of 6 patients, 2 female and 4 male, of which 4 underwent an orbital floor reconstruction and 2 underwent augmentation of other facial skull defects. After 1 year, the mean volume reduction of the implanted Atlantik was 9.78% (5.75%Y14.06%) and 9.73% (1.45%Y19.7%) for the first and second investigators, respectively. The absolute volume reduction in 1 year was 0.38 cm3 (range. 0.10Y0.69 cm3), which resulted in an overall volume reduction of 9.8% of the implanted Atlantik. The Pearson correlation test was 0.996 with a significance level of P G 0.01, and the ICC was 0.998 with a 95% confidence interval between 0.992 and 0.999 This means that the measurements of investigators 1 and 2 nearly matched. Both test results therefore indicate that an OsiriX CT image analysis is very well reproducible (Table 1).

DISCUSSION The aim of this study was to investigate the application and long-term (91 year) stability of Atlantik for secondary orbital floor augmentation and the repair of facial defects. A reduction of the applied Atlantik volume was found being around 10% after more than 1 year. The cases with a longer evaluation time did not show more resorption or impaction of the material. This suggests that the applied volume of the material is partially reduced in the early postoperative period and after this period probably will be stable. Therefore, an overcorrection of bTCP-HA mixture is advised. The Pearson correlation test was 0.996 with a significance level of P G 0.01, and the ICC was 0.998 with a 95% confidence interval between 0.992 and 0.999 This means that the measurements of investigators 1 and 2 nearly matched. Both test results therefore

TABLE 1. Patients and Measurements

Sex Male Male Female Male Male Female Mean (SD)

First Postoperative CT, d

Second Postoperative CT, d

Initial Volume 1st Investigator, cm3

Initial Volume 2nd Investigator, cm3

100 3 78 18 83 25 51.17 (40.55)

783 370 450 368 368 390 454.83 (163.83)

5.98 8.14 3.89 2.84 2.87 1.37 4.18 (2.47)

5.29 7.89 3.30 2.87 2.58 1.32 3.88 (2.35)

Volume Reduction 1st Investigator, cm3/% 0.69 0.47 0.41 0.28 0.21 0.19 0.3728 (0.19)

11.44 5.75 10.55 9.70 7.16 14.06 9.78 (2.99)

Volume Reduction 2nd Investigator, cm3/% 0.10 0.54 0.05 0.50 0.29 0.26 0.2878 (0.21)

1.71 7.35 1.49 17.31 11.40 19.67 9.82 (7.71)

The measuring results of both investigators. Measurements were done using OsiriX.

* 2014 Mutaz B. Habal, MD

Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.

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Bittermann et al

indicate that an OsiriX CT image analysis is very well reproducible. This article also shows the applicability of OsiriX in evaluating bone and implant volumes and its independence of the observer. Previous studies showed an osteoconductive capacity of HA only with micropores.5,9 If large micropores exist, bone ingrowth occurs within the HA. With small micropores, the bone grows only around the implanted HA.11 As Atlantik has large micropores, its osteoconductive capacity is explained. When bTCP is added to the HA, there will be more formation of bone as the bTCP will be resorbed, and bone will grow to replace the bTCP.12 We hypothesize that this process of bTCP-replacement by bone explains the reduction of the volume and increase in bone density, as bTCP is resorbed quickly by the human body, assumed to be around 95% after 48 days.6 A volume reduction of only 10% and not 30%, as would be expected because of the HA:BTCP ratio of 7:3, might be explained by both the quick replacement by bone because of the large micropore structure of the HA and possible osteoinductive properties of bTCP.7,6 Autologous bone is widely used to reconstruct defects in the human body, to avoid unwanted reactions from implanted foreign material. For years, the use of autologous bone has been the criterion standard in reconstruction of the orbital floor and other craniofacial defects. However, with the development of new biocompatible products, the rules for reconstruction of the craniofacial area have changed.13 Adverse effects of autologous bone are an extra in donorsite operation, with related higher risk of infection, longer surgery time, and more blood loss and pain, resulting in a longer recovery period for the patient.10,14 Moreover, the stability of volume and shape of autologous bone is limited, with unpredictable and sometimes even complete resorption of the implanted volume.15 Velich et al16 demonstrated that HA mixtures can be safely applied in sinus floor elevation with satisfactory results, despite its risk of bacterial contamination. There are many other products available on the market for reconstruction of craniofacial defects. Polydioxanone is widely used for the reconstruction of the orbital floor.14 However, this material is completely resorbed, which makes it useful only for bridging small fractures in primary orbital floor reconstruction and not suitable for volume augmentation. Titanium mesh is especially indicated in primary reconstruction of the orbital floor. In secondary repair, it is indicated only if a stable orbital floor on which, for example, the bTCP-HA granules can be placed is missing.1,17 Disadvantages of titanium are possible late perforations or infection of the mesh and the possibility of migration or loosening of the implant.18 The OsiriX open-source program is free and proved easy to use in calculating the volumes of implanted Atlantik. We are not aware of other similar free programs.

CONCLUSIONS A 7:3 HA:bTCP ceramic mixture (Atlantik) is a stable osteoconductive material for the repair of various craniofacial defects. There is a reduction of only 10% of the augmented volume in the long term, which proves it to be potentially useful in repairing orbital floor defects and the resurfacing of the craniofacial skeleton. The material is easy to use, and its application does not require special preparations during operation as volume calculations can be done in advance. Moreover, we confirm the easy applicability and reproducibility of OsiriX in calculating craniofacial augmented bone volumes.

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ACKNOWLEDGMENT The authors thank M. H. Frank, MD, DMD, Department of Oral and Maxillofacial Surgery; University Medical Center Utrecht, the Netherlands, for help with the statistical analysis.

REFERENCES 1. Kuttenberger JJ, Hardt N. Long-term results following reconstruction of craniofacial defects with titanium micro-mesh systems. J Craniomaxillofac Surg 2001;29:75Y81 2. Neumann A, Kevenhoerster K. Biomaterials for craniofacial reconstruction. GMS Curr Top Otorhinolaryngol Head Neck Surg 2009;8:1Y17 3. Baino F. Biomaterials and implants for orbital floor repair. Acta Biomater 2011;7:3248Y3266 4. Yuan H, Fernandes H, Habibovic P, et al. Osteoinductive ceramics as a synthetic alternative to autologous bone grafting. Proc Natl Acad Sci USA 2010;107:13614Y13619 5. Oberg S, Kahnberg KE. Combined use of hydroxy-apatite and Tisseel in experimental bone defects in the rabbit. Swed Dent J 1993;17: 147Y153 6. Gosain AK, Song L, Riordan P, et al. A 1-year study of osteoinduction in hydroxyapatite-derived biomaterials in an adult sheep model: part I. Plast Reconstr Surg 2002;109:619Y630 7. Gosain AK, Riordan PA, Song L, et al. A 1-year study of osteoinduction in hydroxyapatite-derived biomaterials in an adult sheep model: part II. Bioengineering implants to optimize bone replacement in reconstruction of cranial defects. Plast Reconstr Surg 2004;114:1155Y1163Y discussion 1164Y1165 8. Yamada S, Heymann D, Bouler JM, et al. Osteoclastic resorption of calcium phosphate ceramics with different hydroxyapatite/beta-tricalcium phosphate ratios. Biomaterials 1997;18:1037Y1041 9. Alonso N, Tanikawa DY, Freitas Rda S, et al. Evaluation of maxillary alveolar reconstruction using a resorbable collagen sponge with recombinant human bone morphogenetic protein-2 in cleft lip and palate patients. Tissue Eng C Methods 2010;16:1183Y1189 10. Shirota T, Kurabayashi H, Ogura H, et al. Analysis of bone volume using computer simulation system for secondary bone graft in alveolar cleft. Int J Oral Maxillofac Surg 2010;39:904Y908 11. Chim H, Gosain AK. Biomaterials in craniofacial surgery: experimental studies and clinical application. J Craniofac Surg 2009;20:29Y33 12. Gosain AK, Riordan PA, Song L, et al. A 1-year study of hydroxyapatite-derived biomaterials in an adult sheep model: III. Comparison with autogenous bone graft for facial augmentation. Plast Reconstr Surg 2005;116:1044Y1052 13. Kirby EJ, Turner JB, Davenport DL, et al. Orbital floor fractures: outcomes of reconstruction. Ann Plast Surg 2011;66:508Y512 14. Gierloff M, Seeck NGK, Springer I, et al. Orbital floor reconstruction with resorbable polydioxanone implants. J Craniofac Surg 2012;23: 161Y164 15. Tieghi R, Consorti G, Clauser LC. Contouring of the forehead irregularities (washboard effect) with bone biomaterial. J Craniofac Surg 2012;23:932Y934 16. Velich N, Nemeth Z, Toth C, et al. Long-term results with different bone substitutes used for sinus floor elevation. J Craniofac Surg 2004;15: 38Y41. 17. Kozakiewicz M, Elgalal M, Loba P, et al. Clinical application of 3D pre-bent titanium implants for orbital floor fractures. J Craniomaxillofac Surg 2009;37:229Y234 18. Magana FG, Arzac RM, De Hilario Aviles L. Combined use of titanium mesh and resorbable PLLA-PGA implant in the treatment of large orbital floor fractures. J Craniofac Surg 2011;22:1991Y1995

* 2014 Mutaz B. Habal, MD

Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.

One-year volume stability of human facial defects filled with a β-tricalcium phosphate-hydroxyl apatite mixture (Atlantik).

We investigated the applicability and 1-year stability of a β-tricalcium phosphate-hydroxyl apatite mixture (Atlantik) for secondary reconstruction of...
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