Maxillary Sinus Floor Augmentation Using Biphasic Calcium Phosphate: A Histologic and Histomorphometric Study Laurent Ohayon, DDS1 Purpose: The aim of this study was to analyze the histologic quality and histomorphometric quantity of newly formed bone and the biologic properties after maxillary sinus floor augmentation with biphasic tricalcium phosphate (BCP) prior to dental implant placement. Materials and Methods: The selected alloplastic bone substitute, a blend of 60% hydroxyapatite and 40% β-tricalcium phosphate, was placed into the sinus cavity and covered with a bioresorbable membrane. Ten bone samples were harvested from the grafted sinuses of eight patients at 6 months postsurgery for histologic and histomorphometric analysis during implant placement at stage-two surgery. Results: Histologic analysis of the 10 biopsy specimens showed remaining BCP particles in intimate contact with the newly formed bone. Several areas of bone substitute resorption and new bone remodeling were observed. The mean composition of the bone samples harvested from the grafted sinuses was 26.1% ± 6.3% newly formed bone, 29.3% ± 9.1% remaining BCP particles, and 44.7% ± 7.7% connective tissue/bone marrow. Conclusion: BCP biomaterial was osteoconductive and biocompatible. This biomaterial scaffold promoted the formation of new bone, which was in intimate contact with the remaining bone substitute particles. Within the limits of this study, maxillary sinus floor augmentation using BCP bone substitute is a reliable procedure for dental implant placement. Int J Oral Maxillofac Implants 2014;29:1143–1148. doi: 10.11607/jomi.3422 Key words: beta-tricalcium phosphate, bone substitute, histology, histomorphometry, hydroxyapatite, sinus floor augmentation

M

axillary sinus floor augmentation procedures have been developed to recover sufficient crestal bone height for implant placement. This protocol has been evaluated in numerous systematic reviews of the treatment of severely resorbed posterior maxillae.1,2 Autogenous grafts represent the  gold standard,3,4 in terms of bone reconstruction, given that the harvested bone is the only biomaterial offering simultaneous osteoinductive, osteoconductive, and osteogenic properties. However, the need for a second surgical site to harvest the bone graft results in numerous disadvantages, ie, risks of hemorrhage, morbidity, edema, and postsurgical pain.5 Moreover, the limited quantity of bone available intraorally may oblige the surgeon to perform more invasive procedures to harvest extraoral bone from the iliac crest or calvarium under general anesthesia. These harvested autologous bone blocks are then ground into fine particles before being placed 1Private

Practice, Saint Maur des Fosses, France.

Correspondence to: Dr Laurent Ohayon, 25, rue de la Varenne, 94100 Saint Maur des Fosses, France. Fax: +33-1-48-85-09-68. Email: [email protected] ©2014 by Quintessence Publishing Co Inc.

inside the sinus cavity.6 Furthermore, autogenous bone grafting is associated with unpredictable but likely resorption because of the different embryologic origins of the harvested bone and the recipient site bone.7,8 The use of bone substitutes for maxillary sinus floor augmentation offers an interesting alternative to autologous bone grafting, given that it does not require a surgical donor site and these substitutes are available in unlimited quantities. These biomaterials, which may be allografts,9,10 alloplast biomaterials,11,12 or xenografts,13,14 must offer safety, biocompatibility, bioresorbability, and osteoconductivity. The purpose of this article was to analyze the histologic and histomorphometric behavior of an alloplastic bone substitute, Bone Ceramic (Straumann), which is a biphasic calcium phosphate (BCP) composed of 60% hydroxyapatite (HA) and 40% β-tricalcium phosphate (β-TCP) and can be used for maxillary sinus floor augmentation.

MATERIALS AND METHODS Patient Selection

Eight patients (2 men and 6 women between 53 and 68 years of age) with unilateral or bilateral maxillary The International Journal of Oral & Maxillofacial Implants 1143

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posterior edentulism with pronounced pneumatization were scheduled for maxillary sinus floor augmentation. The patients were selected, after preoperative computed tomography scanning, on the basis of a subsinus crestal bone height < 3 mm that would require two surgery procedures with the lateral window procedure prior to implant-supported prosthesis treatment. A 100% BCP bone substitute was used for the surgical procedure. All patients were in generally good health. Excluded were those with: (1) systemic medical contraindications to implant treatment, (2) sinus infection, (3) acute or chronic sinusitis, (4) a smoking habit of < 10 cigarettes per day,15 (5) a history of bisphosphonate treatment, (6) previous irradiation of the head and neck, (7) uncontrolled diabetes, and/or (8) current pregnancy or lactation. The study described in this report was performed in accordance with the rules specified in the Declaration of Helsinki on experimentation involving human subjects. The patients were informed of the possible risks and benefits of the surgical protocol and treatment alternatives before signing a written consent form.

Surgical Protocol

All sinus floor augmentation surgeries were performed with the same lateral bone window technique.16 Under local anesthesia with a vasoconstrictor delivered buccally and palatally, a crestal incision was performed slightly palatally along the crestal bone throughout the total length of the edentulous zone. Two buccal vertical releasing incisions were placed mesially and distally. A full-thickness flap was elevated to expose the alveolar crest and the lateral sinus wall. A bone window was performed by ostectomy using a round bur mounted on a contra-angle with sterile saline solution irrigation. The bone window was meticulously fractured and rotated medially inside the sinus cavity. The sinus membrane was carefully elevated from the lateral, inferior, and medial bone walls of the sinus cavity with curettes of different shapes to prevent damage. The horizontally repositioned bone window represented the new sinus floor cavity and the upper limit of the grafted bone ridge. The BCP was then placed and gently condensed inside the space obtained by the separation of the membrane from the sinus walls, starting at the anterior and posterior parts and finishing at the medial part of the grafted cavity. Two different bioabsorbable membranes were used as cell-occlusive barriers to cover the buccal window.17 The first was a synthetic glycolide and trimethylene carbonate copolymer fiber membrane (Gore Resolut Adapt, Gore), and the second was a collagen membrane containing types I and III porcine native collagen (Bio-Gide, Geistlich). The full-thickness flap was repositioned and

closed without tension with horizontal mattress and interrupted sutures to obtain primary closure. Patients received 1 g amoxicillin with clavulanic acid twice a day for 8 days starting 1 hour before surgery, as well as 1 mg/kg prednisolone anti-inflammatory medication once a day for 5 days to reduce postoperative swelling. Antiseptic oral rinses (0.12% chlorhexidine digluconate twice daily beginning the day after surgery) and paracetamol for pain control were prescribed. Sutures were removed after 2 weeks. The patients were asked to avoid sneezing or blowing their nose during the 2-week postoperative period to prevent interference with healing of the elevated sinus membrane.

Histologic Processing

At 6 months postoperative, during stage-two surgery, harvesting of bone samples, preferably in the area of the first molar implant, was done to carry out histologic and histomorphometric analyses. After elevation of a full-thickness flap, bone samples were harvested using 2.4-mm internal-diameter trephines. The bone cores were first fixed in a Bouin solution, after the exclusion of any residual crestal native bone from the coronal portion, and then soaked in a 14% nitric acid–free hydrochloride solution to accomplish light and rapid decalcification. This allowed sectioning of the bone samples with a microtome without damaging the cells or the newly formed bone tissue, which was very poorly calcified at this stage. The samples were immersed again in a Bouin solution to confirm the fixation, then dehydrated and coated in paraffin.18 The coated cores were sliced with a microtome and reduced by microgrinding and polishing to obtain 5-µm-thick sections.19 Staining was performed using hematein-eosin-Safran trichrome, which optimizes visualization of the different components of connective and bone tissue. Bone sample sections were examined with a BX 51 light microscope (Olympus) at several different magnifications.

Histomorphometric Processing

The histomorphometric evaluation process was performed at low magnification on the entire surface of the bone sample histologic sections using a digital camera DFW-X710 (Sony) connected to a Mirax-scan (Zeiss) image analyzer. Color coding of newly formed bone, remaining BCP particles, and connective tissue/ bone marrow allowed the clear identification and accurate quantification of each investigated part. The histomorphometric analyses were performed on the bone samples, which had been harvested through the residual subsinus crestal bone from the grafted sinuses. Therefore, these native sinus crestal bone ridges, which constituted the preoperative

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residual sinus floor, were removed from all bone samples before evaluation to obtain more precise percentage data of the grafted bone component.

BC

NB

NB

Polarized Light Microscopy

The orientation of newly formed bone collagen fibers around the remaining BCP particles was analyzed under polarized light. Polarized light is refracted differently depending on the orientation of new bone collagen fibers. If they are oriented parallel to the plane of section, they will appear whitish-yellow because of the modification via refraction of the light source, whereas if they are oriented perpendicular to the plane section, they appear dark gray because of a lack of refraction of the polarized light. New bone collagen fibers with an angled orientation appear yellowish-orange. Remaining bone substitute particles do not refract light and thus appear black because of the total absence of a collagen component.

BC CT NB

BC

BC

BC

BC

CT CT

NB

Fig 1   Histologic section of a bone sample under light microscopy (magnification ×20). BC = BCP; NB = newly formed bone; CT = connective tissue/bone marrow. NB CT

NB

RESULTS

BC

Clinical and Tomographic Findings

A total of 10 sinus floor augmentations were performed in eight patients. Preoperatively, the residual subsinus bone ridge of each treated sinus was less than 3 mm high. No complications were observed during the 6-month healing period, except for a 3-day minor nosebleed in one patient. Sufficient graft volumes were obtained according to the 6-month postoperative computed tomographic scans to enable implant placement. Twenty-four Ti-Unite rough-surface implants (Nobel Biocare) were inserted in the grafted sinuses at 6 months postoperative. The implants were uncovered and loaded 4 months after stage-two surgery with fixed prostheses. No early or late implant failures were observed, and a 100% prosthetic survival rate was obtained for the 25 implants inserted into the grafted sinuses after 1 to 4 years in function. These data confirmed the success rate reported by a previous study at 1 year after implant loading following maxillary sinus floor augmentation using BCP.20

Light Microscopic Observations

In all but one patient, who received one implant in the second premolar area, specimens were harvested from the first molar area. The histologic analysis at ×20 magnification (Fig 1) showed large-scale views of the bone cores. The BCP particles were integrated into the newly formed bone, and several areas of bone substitute resorption and new bone remodeling were observed. These two mineralized structures were in close contact and surrounded by the marrow, which was a fibrous, richly vascularized nonhematopoietic

CT

Fig 2  Histologic section (magnification ×100). Newly formed bone (NB) presents a trabecular aspect. Resorption activity of osteoclastlike multinucleated cells around the BCP residual particles (BC) was clearly observed. CT = connective tissue/bone marrow; arrowheads = osteocytes; black arrows = osteocytes; white arrows = osteoid border.

regenerative connective tissue. The remaining BCP particles were distributed homogeneously on the surface of the sample. No acute or chronic inflammatory cell infiltrate was observed, which confirmed the biocompatibility of the bone substitute. Light microscope images obtained at ×100 magnification (Fig 2) allowed clear identification of the newly formed bone, which showed large areas with contours clearly delimited by a darker line, ie, the osteoid border. The osteoid border was composed of osteoblasts, which control bone mineralization and synthetize the extracellular organic matrix, ie, the osteoid substance. Osteoclast-like multinucleated giant cells were present in large quantities around the bone substitute particles, thus confirming the intense resorption process of the bone substitute. Histologic specimens observed at ×400 magnification (Fig 3) focused on the close contact between the remaining BCP particles and the new bone. The oriented lamellar bone trabeculae were easily identified. Pyknotic cells (osteocytes) were embedded within the bone mineral matrix. The International Journal of Oral & Maxillofacial Implants 1145

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NB

BC NB BC Fig 3  Light microscopy histologic section (magnification ×400). Blood vessels (white arrowheads), delimited by endothelial cells, were surrounded by connective tissue sleeves within the newly formed bone area (NB). Inflammatory cells (black arrowheads), dispersed within the bone substitute (BC), highlighted the resorption process of the biomaterial. NB was in contact with the BC without any gaps. Numerous osteocytes (black arrows) were identified within the NB mineralized matrix. NB in the process of remodeling appeared within the remaining BC. White arrows = osteoclasts.

Histomorphometric Findings

At 6 months postoperative, the mean percentages of the 10 bone samples harvested from the grafted sinuses during stage-two implant placement surgery were 26.1% ± 6.3% newly formed bone, 29.3% ± 9.1% remaining BCP particles, and 44.7% ± 7.7% connective tissue/bone marrow (Table 1).

Polarized Light Observations

The same areas of the bone samples were examined under polarized light (Fig 4) and compared to the light microscopic images at the same magnification to correlate the volume and quality of new bone and highlight the orientation of collagen fibers. BCP particles were surrounded by lamellar bone with collagen fibers randomly oriented. The new bone trabeculae were clearly outlined with smaller areas of immature bone, thus demonstrating the high level of calcification of the bone graft at this stage of healing.

DISCUSSION BCP is composed of a blend of two alloplastic biomaterials, HA and β-TCP. These two synthetic materials have been used individually for several years,21–23 and their usefulness for sinus grafting has already been mentioned in numerous publications.24,25 They have demonstrated biocompatibility (ie, their capacity to change themselves into nontoxic molecules that the body may

then metabolize or eliminate) and osteoconduction (which ensures optimal bone integration as well as a potential to generate new bone), qualities that contribute toward physiologic remodeling to change the newly formed fibrillar bone into lamellar bone. HA and β-TCP, both derived from calcium phosphate, also have specific physical and chemical properties; they are blended in specific proportions to increase the bone reconstructive qualities of the new bone substitute thus obtained.26 The HA/β-TCP ratio, which constitutes this BCP, is not obtained by mixing particles of each individual component. The production principle of this biomaterial allows a constant ratio of 60% HA and 40% β-TCP to be obtained by chemical synthesis during its initial production phase. The two components therefore become part of the same crystal and are thus distributed in a uniform and homogenous manner within the obtained blocks of BCP. These blocks are then ground into particles ranging between 0.5 and 1 mm in size, which will each be composed of the same HA/β-TCP ratio. The rapid resorption properties of β-TCP27,28 allow bone cell colonization and the creation of space for the newly formed bone, while HA, which resorbs more slowly,29 forms the scaffold required to maintain the obtained volume throughout the period of new bone formation and remodeling.30 The remaining particles of BCP were fully integrated into the newly formed bone network.28 Therefore, the partially resorbed BCP was replaced by lamellar bone,31 which distinguished the mature bone from less mature areas. The quantitative evaluation of new bone formation confirmed the mean amounts of newly formed bone reported by earlier studies of 27.3% and 26.4%, respectively.32,33 The newly formed bone was in close contact with bone substitute, highlighting the osteoconductive properties of the BCP. BCP may constitute an osteoconductive scaffold to support new bone formation. The resorption process of the BCP occurs through physicochemical dissolution by the biologic fluids of the material into small particles, which will be phagocytized by the osteoclasts.34,35 The porosity of BCP is approximately 90%, resulting in macropores ranging from 100 to 500 µm in size; the term porosity corresponds to the sum of microporosity and macroporosity and characterizes the biomaterial. Macroporosity refers to the scaffold of the material.36 The size of the macropores, as well as their interconnections and the presence of micropores,37 can promote the penetration and proliferation of blood vessel buds, which will carry the osteoprogenitor cells to generate new bone formation. In addition, the presence of micropores within the macroporous wall increases the specific surface area to make the BCP osteoinductive.38

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Ohayon

Table 1  Histomorphometric Findings in Biopsy Specimens Composition of biopsy specimens Sex

Age (y)

1

M

59

R L

15-16-17 26-27

2

M

68

R

3

F

53

R

Patient no.

Side

Implant position(s)*

Biopsy area (mm2)

New bone (%)

21.8 16.7

36.1 18.1

17

16.6

16-17

23.7

BCP (%)

CT/BM (%)

19.5 34.6

44.4 47.3

34.2

29.1

36.7

19.2

38.5

42.6

4

F

59

R

14-15-16-17

20.8

22.7

24.5

52.8

5

F

61

R

14-15-16

19.9

24.8

19.7

55.5

6

F

55

R L

16-17 24-25-26-27

19.5 13.5

20.7 22.2

49.6 27.9

29.7 49.9

7

F

73

L

26

18.7

32.5

29.8

37.7

8

F

62

R

16-17

15.5

30.4

19.6

50.0

Mean ± SD

18.7 ± 2.7

26.1 ± 6.3

29.3 ± 9.1

44.7 ± 7.7

CT/BM = connective tissue/bone marrow; SD = standard deviation. *FDI tooth-numbering system; bolded numbers indicate location of the harvested bone core.

CONCLUSION Biphasic calcium phosphate as a bone substitute presents with biocompatibility and osteoconductive properties, as confirmed by this histologic analysis. The association of hydroxyapatite (HA) and beta-tricalcium phosphate (β-TCP) in the indicated ratio of 60/40 combines the persistence of HA to maintain the bone volume during the period of bone healing with the faster resorption of the β-TCP to facilitate new bone formation. The biphasic calcium phosphate biomaterial examined here (HA/β-TCP, 60/40), within the limitations of this study, allows the new bone formation necessary for implant treatment in the case of sinus floor augmentation procedures.

ACKNOWLEDGMENTS The author would like to thank Dr Marie-Dominique Bruneau, M. Vincent Verger, and M. Gilles Le Naour, Department of Oral Pathology and Maxillofacial Surgery, Pitie-Salpetriere-Hospital of Paris, for the preparation of the histologic sections and the histomorphometric evaluation, and Dr Bernard Fromenty, Research Director, National Institute of Health and Medical Research, Research Department of Rennes, for his expertise and professional assistance. No financial support was received for this study. The authors reported no conflicts of interest related to this study.

REFERENCES 1. Del Fabbro M, Testori T, Francetti L, Weinstein R. Systematic review of survival rates for implants placed in the grafted maxillary sinus. Int J Periodontics Restorative Dent 2004;24:565–577.

BC

BC CT

NB

CT

BC

NB BC BC NB

Fig 4  Histologic section under polarized light (magnification ×20). The colors of the new bone (NB) collagen fibers, when observed under polarized light, changed from whitish-yellow to yellowish-orange to dark gray, depending on their orientation. The collagen fibers of the lamellar bone (black arrows) were randomly oriented as in woven bone. BC = BCP bone substitute; CT = connective tissue/bone marrow.

2. Nkenke E, Stelzle F. Clinical outcomes of sinus floor augmentation for implant placement using autogenous bone or bone substitutes: A systematic review. Clin Oral Implants Res 2009;20(suppl 4):124–133. 3. Cordaro L. Bilateral simultaneous augmentation of the maxillary sinus floor with particulated mandible. Report of a technique and preliminary results. Clin Oral Implants Res 2003;14:201–206. 4. Jensen OT, Leopardi A, Gallegos L. The case for bone graft reconstruction including sinus grafting and distraction osteogenesis for the atrophic edentulous maxilla. J Oral Maxillofac Surg 2004;62:1423–1428. 5. Bahat O, Fontanessi RV. Complications of grafting in the atrophic edentulous or partially edentulous jaw. Int J Periodontics Restorative Dent 2001;21:487–495. 6. Le Lorc’h-Bukiet I, Tulasne JF, Llorens A, Lesclous P. Parietal bone as graft material for maxillary sinus floor elevation: Structure and remodeling of the donor and of recipient sites. Clin Oral Implants Res 2005;16:244–249.

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24. Artzi Z, Nemcovsky CE, Tal H, Dayan D. Histopathological morphometric evaluation of 2 different hydroxyapatite-bone derivatives in sinus augmentation procedures: A comparative study in humans. J Periodontol 2001;72:911–920. 25. Schopper C, Moser D, Sabbas A, et al. The fluorohydroxyapatite (FHA) FRIOS Algipore is a suitable biomaterial for the reconstruction of severely atrophic human maxillae. Clin Oral Implants Res 2003;14:743–749. 26. Nery EB, Le Geros RZ, Lynch KL, Lee K. Tissue response to biphasic calcium phosphate ceramic with different ratios of HA/beta TCP in periodontal osseous defects. J Periodontol 1992;63:729–735. 27. Arinzeh TL, Tran T, Mcalary J, Daculsi G. Comparative study of biphasic calcium phosphate ceramics for human mesenchymal stem-cell induced bone formation. Biomaterials 2005;26:3631–3638. 28. Jensen SS, Broggini N, Hjørting-Hansen E, Schenk R, Buser D. Bone healing and graft resorption of autograft, anorganic bovine bone and beta-tricalcium phosphate. A histologic and histomorphometric study in the mandibles of minipigs. Clin Oral Implants Res 2006;17:237–243. 29. Jensen SS, Yeo A, Dard M, Hunziker E, Schenk R, Buser D. Evaluation of a novel biphasic calcium phosphate in standardized bone defects. A histologic and histomorphometric study in the mandibles of minipigs. Clin Oral Implants Res 2007;18:752–760. 30. Detsch R, Mayr H, Ziegler G. Formation of osteoclast-like cells on HA and TCP ceramics. Acta Biomater 2008;4:139–148. 31. Daculsi G, Weiss P, Bouler JM, Gauthier O, Millot F, Aguado E. Biphasic calcium phosphate/hydrosoluble polymer composites: A new concept for bone and dental substitution biomaterials. Bone 1999;25(2 suppl):59S–61S. 32. Frenken JW, Bouwman WF, Bravenboer N, Zijderveld SA, Schulten EA, ten Bruggenkate CM. The use of Straumann Bone Ceramic in a maxillary sinus floor elevation procedure: A clinical, radiological, histological and histomorphometric evaluation with a 6-month healing period. Clin Oral Implants Res 2010;21:201–208. 33. Kolerman R, Goshen G, Joseph N, Kozlovsky A, Shetty S, Tal H. Histomorphometric analysis of maxillary sinus augmentation using an alloplast bone substitute. J Oral Maxillofac Surg 2012;70:1835–1843. 34. Yamada S, Nakamura T, Kokubo T, Oka M, Yamamuro T. Osteoclasic resorption of apatite formed on apatite and wollastonite containing glass-ceramic by simulated body fluid. J Biomed Mater Res 1994;28:1357–1363. 35. Daculsi G, Bouler JM, Legeros RZ. Adaptive crystal formation in normal pathological calcifications in synthetic calcium phosphate related biomaterials. Int Rev Cytol 1997;172:129–191. 36. Fleckenstein KB, Cuenin MF, Peacock ME, et al. Effect of a hydroxyapatite tricalcium phosphate alloplast on osseous repair in the rat calvarium. J Periodontol 2006;77:39–45. 37. Hornez JC, Chai F, Monchau F, Blanchemain N, Deschamps M, Hildebrand. HF. Biological and physico-chemical assessment of hydroxyapatite (HA) with different porosity. Biomol Eng 2007;24:505–509. 38. Habibovic P, Sees TM, van den Doel MA, van Blitterswijk Ca, de Groot K. Osteoinduction by biomaterials—Physicochemical and structural influences. J Biomed Mater Res A 2006;77:747–762.

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Maxillary sinus floor augmentation using biphasic calcium phosphate: a histologic and histomorphometric study.

The aim of this study was to analyze the histologic quality and histomorphometric quantity of newly formed bone and the biologic properties after maxi...
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