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259

Maxillary Sinus Grafting with a Synthetic, Nanocrystalline Hydroxyapatite-Silica Gel in Humans: Histologic and Histomorphometric Results

Dieter D. Bosshardt, PhD1/Michael M. Bornstein, PD Dr Med Dent2 Jean-Pierre Carrel, Dr Med Dent3/Daniel Buser, Prof Dr Med Dent1 Jean-Pierre Bernard, Prof Dr Med Dent4 The aim of this study was to evaluate in humans the amount of new bone after sinus floor elevation with a synthetic bone substitute material consisting of nanocrystalline hydroxyapatite embedded in a highly porous silica gel matrix. The lateral approach was applied in eight patients requiring sinus floor elevation to place dental implants. After elevation of the sinus membrane, the cavities were filled with 0.6-mm granules of nanocrystalline hydroxyapatite mixed with the patient’s blood. A collagen membrane (group 1) or a platelet-rich fibrin (PRF) membrane (group 2) was placed over the bony window. After healing periods between 7 and 11 months (in one case after 24 months), 16 biopsy specimens were harvested with a trephine bur during implant bed preparation. The percentage of new bone, residual filler material, and soft tissue was determined histomorphometrically. Four specimens were excluded from the analysis because of incomplete biopsy removal. In all other specimens, new bone was observed in the augmented region. For group 1, the amount of new bone, residual graft material, and soft tissue was 28.7% ± 5.4%, 25.5% ± 7.6%, and 45.8% ± 3.2%, respectively. For group 2, the values were 28.6% ± 6.90%, 25.7% ± 8.8%, and 45.7% ± 9.3%, respectively. All differences between groups 1 and 2 were not statistically significant. The lowest and highest values of new bone were 21.2% and 34.1% for group 1 and 17.4% and 37.8% for group 2, respectively. The amount of new bone after the use of nanocrystalline hydroxyapatite for sinus floor elevation in humans is comparable to values found in the literature for other synthetic or xenogeneic bone substitute materials. There was no additional beneficial effect of the PRF membrane over the non-cross-linked collagen membrane. (Int J Periodontics Restorative Dent 2014;34:259–267. doi: 10.11607/prd.1419)

Professor, Department of Oral Surgery and Stomatology, School of Dental Medicine, University of Bern, Bern, Switzerland.

1

Senior Lecturer, Department of Oral Surgery and Stomatology, School of Dental Medicine, University of Bern, Bern, Switzerland.

2

Senior Lecturer, Department of Stomatology and Oral Surgery, School of Dental Medicine, University of Geneva, Geneva, Switzerland.

3

The successful placement of a dental implant in jawbone requires sufficient width and height of bone at the recipient site. In many patients, however, a bone augmentation procedure is indicated. Autogenous bone is still considered the gold standard in osseous reconstructive surgery because of its osteoinductive, osteoconductive, and osteogenic properties.1–3 However, disadvantages of autogenous bone include donor site morbidity, limited availability, and increased surgical time. To reduce the shortcomings of autograft harvesting, various bone substitute materials have been used alone or in combination with autogenous bone. Bone substitute materials must fulfill certain criteria such as biocompatibility, osteoconductivity, and volume stability. Human histology is needed to confirm results derived from

Professor, Department of Stomatology and Oral Surgery, School of Dental Medicine, University of Geneva, Geneva, Switzerland.

4

Correspondence to: Prof Dieter D. Bosshardt, University of Bern, School of Dental Medicine, Department of Oral Surgery and Stomatology, CH-3010, Bern, Switzerland; fax: +41 31 6323941; email: [email protected]. ©2014 by Quintessence Publishing Co Inc.

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260 animal experiments when testing new biomaterials. In this regard, the augmentation of the maxillary sinus has proven to be advantageous since a staged sinus floor elevation procedure may be indicated prior to implant placement,4 and a core biopsy cylinder can be harvested at the time of implant placement. Human histologic and histomorphometric data of biopsy specimens retrieved from the augmented maxillary sinus exist for autografts,5 allografts,6,7 xenografts,8–10 alloplastic calcium phosphate biomaterials,9,10 alloplastic glass materials,11 recombinant human growth factors,12,13 plateletrich plasma,14 and combinations of biomaterials.15,16 Despite tremendous research efforts, it appears that the ideal bone substitute or composite material has still not been found. Regarding recently developed alloplastic biomaterials, there is a lack of information concerning their potential to support new bone formation and maintain the gained bone volume. One such synthetic biomaterial consists of nanocrystalline hydroxyapatite embedded in a highly porous silica gel matrix (NanoBone, Artoss). Animal experiments have shown that the silica gel matrix rapidly degrades and becomes replaced by an organic material.17 Furthermore, complete bone formation and almost complete biomaterial resorption were observed in critical-size defects in miniature pigs.18 Data from human biopsy materials are very rare. In a study with 16 patients, where this biomaterial was used for sinus floor eleva-

tion, it was shown that 6 months after grafting, 48% of the grafted area consisted of new bone.19 This very high bone density largely exceeds those obtained with other bone substitute materials.9,10,20 The aim of this study was to evaluate in humans the amount of new bone after sinus floor elevation with a synthetic bone substitute material consisting of nanocrystalline hydroxyapatite. Biopsy specimens harvested at the time of implant placement were histologically and histomorphometrically analyzed.

Method and materials Surgical procedure

Eight patients (seven women and one man; 41 to 64 years old) referred to the Department of Stomatology and Oral Surgery at the University of Geneva, Geneva, Switzerland, with bone height requiring a staged sinus floor elevation procedure to insert dental implants were included in the study. All patients signed an informed consent form and were treated according to the guidelines in the Declaration of Helsinki. The vertical height of the residual ridge at the edentulous maxilla below the floor of the maxillary sinus was less than 4 mm. Systemic and local factors that could potentially interfere with implant surgery were defined as exclusion criteria; smokers and subjects with acute or chronic sinus disease were excluded from the study.

One hour before surgery, patients received 600 mg clindamycin (Dalacin C, Pfizer) and 500 mg paracetamol (Dafalgan, Bristol-Myers Squibb). Sinus floor elevation surgeries were performed under local anesthesia by infiltration using articaine (Ubistesin, 3M) without sedation. After crestal and mesial oral incisions, a full-thickness mucosal flap was elevated to expose the external sinus wall. A bony window, measuring approximately 10 × 5 mm, was opened with a 3-mm-diameter diamond bur under saline water irrigation. The sinus membrane was carefully elevated from the bony window to the internal sinus wall, and the cavity was filled with 0.6-mm granules of synthetic nanocrystalline hydroxyapatite embedded in a highly porous silica gel matrix (NanoBone) mixed with the patient’s blood. In three patients (four specimens; group 1), a collagen membrane (Bio-Gide, Geistlich) was prepared. In five patients (eight specimens; group 2), a membrane made of platelet-rich fibrin (PRF)21 was prepared chairside and used to cover the lateral window. The mucosal flap was repositioned and sutured with polyamide 5.0 sutures (Suturamid, B. Braun Aesculap). After surgery, Dalacin C (300 mg) was maintained three times a day for 5 days and Dafalgan (500 mg) three to four times per day depending on the degree of pain. Dental hygiene was performed from the first postoperative day by oral rinses with chlorhexidine (0.12%) (Plak Out Gel, KerrHawe) three times a day until suture removal 7 days postsurgery (Fig 1).

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261

a

b

Fig 1    (a) Panoramic view exhibiting the right posterior maxilla with little residual bone height and an extended maxillary sinus. (b) The same patient after staged sinus floor elevation with nanocrystalline hydroxyapatite mixed with the patient’s blood in the right posterior maxilla.

There were no postoperative adverse events recorded, and implant insertion was performed after healing periods of 7 to 11 months following the same preoperative treatment and local anesthesia protocol. In one patient, biopsy specimen retrieval and implant insertion occurred 24 months after sinus floor elevation because the patient was working abroad and wanted to wait for implant insertion upon his return. A crestal incision was performed, and implant bed preparation was achieved using a 3.5-mm-external-diameter hollow drill (Institut Straumann) to harvest the bone core that was then processed for histologic and histomorphometric analyses. A total of 16 biopsy specimens were harvested from eight patients. Afterward, 16 transmucosal titanium implants with a sandblasted and

acid-etched surface and a diameter of 4.1 mm (Institut Straumann) were inserted without pretapping, and suturing was performed. All implants were clinically stable after insertion and were loaded after 12 weeks of uneventful healing.

Histologic procedure

After harvesting, the 16 biopsy specimens were immediately placed in a container filled with a fixative consisting of 1% glutaraldehyde and 1% formaldehyde buffered with 0.08 mol/L sodium cacodylate (pH 7.4). Following fixation for 24 hours at 4°C by immersion, the tissue samples were decalcified in 4.13% disodium ethylenediamine tetraacetic acid (EDTA) for 4 to 6 weeks at 4°C, followed by extensive washing in 0.1 mol/L

sodium cacodylate buffer containing 5% sucrose (pH 7.3). The demineralized samples were subdivided into smaller samples. Longer biopsy cylinders were subdivided into four pieces, whereas shorter cylinders were cut into two halves. All specimens were dehydrated in ascending concentrations of ethanol and processed for embedding in LR White resin (Fluka). This resulted in a total of 54 LR White blocks. Semithin survey sections (1-µm thick) were cut with glass and diamond knives on a Reichert Ultracut E microtome (Leica Micro­ systems), stained with toluidine blue and fuchsin, and observed in a Zeiss Axioplan photomicroscope (Carl Zeiss). Microphotography was performed using a ProgRes C5 digital camera (Jenoptik Laser, Optik, Systeme) connected to a Zeiss microscope (Carl Zeiss).

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262

NB

OB

* BM

NB OB

NB

* NB

a

NB

BM

* NB

Fig 2    (a) The native or old bone (OB) of the residual ridge displays a lamellar matrix structure and mature bone marrow (BM) but no nanocrystalline hydroxyapatite particles. In contrast, new bone (NB) and hydroxyapatite particles (asterisks) but no mature bone marrow are present in the grafted area. (b) In the grafted area shown, which measures 5 mm in length, consolidation of the hydroxyapatite particles has occurred throughout the core biopsy specimen. New bone forms a fine scaffold interconnecting neighboring hydroxyapatite particles. The presence of adipocytes at some sites is indicative of bone marrow development.

*

BM

*

*

NB NB

*

b

Histomorphometric evaluation

Histomorphometric measurements were performed in the augmented region to calculate the percentages (ie, area fraction) of mineralized new bone, residual alloplastic material, and soft tissue component (ie, soft connective tissue/ bone marrow space). The inclusion criterion for measurements was the presence of tissues in the augmented region. Exclusion criteria were absence of augmented region in the biopsy specimen and histologically detectable signs of perforation of the sinus membrane with concomitant inflammation. Measurements were performed in the augmented region, thus excluding the residual ridge. All mea-

surements were determined by point counting directly in the light microscope, using an optically superimposed eyepiece test square grid (distance between 6 × 6 test lines = 255 µm) at a magnification of 160-fold.22 The number of points of intersection between the test lines and the outlines of mineralized bone, bone substitute particles, and nonmineralized tissue compartments were recorded. In a subset of specimens, the histomorphometric analysis was performed twice to determine the reproducibility of the method employed. Descriptive statistics are given as mean ± SD.

Statistical analysis

The initial descriptive analysis of the data was done using box plots for the distribution of the analyzed tissues (bone, filler material, and soft tissue). Means and SDs were calculated for all measurements. Due to the small sample size, the normality of the data within the two groups is hard to verify. Hence, a nonparametric approach for further data analysis was taken. To detect differences between bone volume, filler material, and soft tissue percentages, separate Wilcoxon rank-sum tests were performed. All analyses were done using specialized statistical software (SAS 9.1, SAS Institute). The significance level chosen for all statistical tests was P ≤ .01.

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263 Fig 3    (a) Native bone consists of mature trabecular bone (TB) with large bone marrow (BM) spaces. (b) A higher magnification illustrates a bone trabecula surrounded by bone marrow; note the many cement lines (arrows) interfacing discrete packets of bone, which are characterized by a lamellar matrix pattern.

BM TB

TB BM

TB

TB BM a

* NB

* a

NB

BM

* * NB

*

NB

b

NB

*

NB

* BM

*

BM NB

b

c

Fig 4    (a) Newly formed bone (NB) consists of a fine scaffold of trabeculae, which are in contact with the nanocrystalline hydroxy­apatite particles (asterisks), and an immature bone marrow (BM). (b) The bone trabeculae consist mainly of woven bone reinforced by some parallel-fibered bone. (c) The synthetic hydroxyapatite-silica gel has a heterogeneous matrix texture and is intensely but differently stained from the bone matrix.

Results Twelve of the 16 biopsy specimens were suitable for a histomorphometric analysis (Fig 2). In 4 biopsy specimens, only old bone from the residual ridge was contained in the trephine bur. The following descriptive and histomorphometric results pertain to all remaining 12 specimens. No qualitative differences were observed between groups 1 and 2. The bone of the residual ridge was clearly recognizable and characterized by mature bone trabeculae with interspersed large bone marrow spaces (Figs 2a and 3). In all samples, new bone was observed in the augmented region of the maxillary sinus (Figs 2b and 4 to 6). The newly

formed bone was evenly distributed throughout the augmented region and formed a dense network of trabeculae interconnecting neighboring nanocrystalline hydroxyapatite particles (Figs 2b and 4a). Morphologically, the newly formed bone resembled woven bone, as indicated by the presence of numerous osteocytes and lack of parallel-fibered and lamellar bone matrix (Fig 4c). New bone matrix deposited against cement lines appeared more mature. The newly formed bone was seen in close contact with the nanocrystalline hydroxyapatite particles without any intervening tissue layer or tissue processing artifacts (Fig 4c). The hydroxyapatite particles were structurally inhomogeneous and appeared porous (Figs 4c and 5).

If the surface of the nanocrystalline hydroxyapatite was exposed to the soft tissue, numerous large multinucleated cells were present at the biomaterial–soft tissue interface and many blood vessels were nearby (Figs 5 and 6). Infrequently, cells were observed inside the porous matrix of the hydroxyapatite particles (Fig 5b). The soft tissue itself contained many blood vessels and did (Fig 6b) or did not (Fig 6a) resemble bone marrow, as indicated by the presence of adipocytes. The results of the histomorphometric analysis for all individuals from groups 1 and 2 are shown in Tables 1 and 2, respectively, whereas the mean values ± SDs are illustrated in Fig 7. For group 1, the mean amount of new bone, residual

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264 Fig 5    (a) New bone (NB) is directly deposited onto the synthetic hydroxyapatite-silica gel particles (asterisks). Many multinucleated giant cells (arrows), which resemble osteoclasts, are present at the interface between synthetic graft substitute material and soft tissue/bone marrow. Blood vessels (BV) are typically found in close vicinity to the osteoclast-like cells. (b) Blood vessels, osteoclast-like cells, and other cell types are occasionally found within the synthetic hydroxyapatite-silica gel matrix.

NB

BV NB NB

*

* BV

*

BV

BV

* NB a

b BV

Fig 6    Cement lines (CL), which are indicative of bone remodeling activity, are seen at (a) sites where the soft tissue contains blood vessels (BV) but does not resemble bone marrow and (b) at sites where the presence of blood vessels and adipocytes (AC) is indicative of a more advanced stage of bone marrow (BM) maturation. Multinucleated giant cells (arrows) resembling osteoclasts are omnipresent at the NanoBone–soft tissue interface.

*

* BV

BV

BV CL

AC

NB

*

a

Table 1 Specimen no.

BM

NB

b

Newly formed bone, residual bone substitute material, and soft tissue for group 1 patients Healing period (mo)

Bone (%)

Filler (%)

Soft tissue (%)

1

10

30.35

25.05

44.60

2

8

29.40

27.40

43.20

3

8

21.15

34.00

44.85

4

24

34.05

15.55

50.40

28.74 ± 5.44

25.50 ± 7.64

45.76 ± 3.18

Mean ± SD

filler material, and soft tissue was 28.7% ± 5.4%, 25.5% ± 7.6%, and 45.8% ± 3.2%, respectively. For group 2, the corresponding values

were 28.6% ± 6.9%, 25.7% ± 8.8%, and 45.7% ± 9.3%, respectively. All differences between groups 1 and 2 were not statistically significant.

Discussion Sinus floor elevation with a broad range of filler materials is the most

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265

Table 2

100

Healing period (mo)

Bone (%)

Filler (%)

Soft tissue (%)

1

9

30.65

30.45

38.90

2

9

25.80

30.45

43.75

3

8

31.65

24.80

43.55

4

8

23.70

21.75

54.55

5

11

36.65

15.80

47.55

20

6

11

17.35

20.40

62.25

10

7

10

25.10

43.00

31.90

8

7

37.80

18.70

43.50

28.59 ± 6.90

25.67 ± 8.75

45.74 ± 9.30

Mean ± SD

common surgical intervention for the placement of dental implants in the posterior maxilla23 and is considered a predictable treatment method with high implant success/ survival rates and low incidences of surgical complications.24 All implants in this study were loaded after 12 weeks of uneventful healing. The results show that after sinus floor elevation and augmentation with nanocrystalline hydroxyapatite in humans, new bone consistently formed between the synthetic biomaterial particles in the augmented region of all biopsy samples where complete tissue harvesting was successful, ie, in 75% of all samples. Only four specimens proved to be unsuitable for histologic and histomorphometric analysis due to incomplete tissue removal. This is comparable with another sinus

floor elevation study in humans where an even higher percentage of unsuitable samples occurred.9 The mean percentage of new bone found in the present study for all specimens (ie, groups 1 and 2) was 28.7%. This bone density value is lower than those reported for NanoBone in other sinus floor elevation studies in humans, where bone densities of 37.7% after 8 to 15 weeks25 and 48% after 6 months19 of healing were obtained. The reason for this difference is currently not known. However, it has to be taken into consideration that a recent histomorphometric meta-analysis of sinus floor elevation in humans with various grafting materials showed great variation in bone density, with mean values ranging from 14.7% to 53.5% and large variations be-

90 80

45.76

45.74

25.50

25.67

28.74

28.59

Group 1

Group 2

70 60 %

Specimen no.

Soft tissue Bone filler New bone

Newly formed bone, residual bone substitute material, and soft tissue for group 2 patients

50 40 30

0

Fig 7    Mean area fractions for new bone, residual synthetic bone substitute material, and soft tissue for groups 1 and 2.

tween studies using the same bone filler material.26 Other important influencing factors are the degradation time of the bone filler and the timepoint of sampling after filler implantation.20,27–29 Most studies with autogenous bone alone show that the highest bone densities are reached in an early phase after implantation. In contrast, the amount of new bone in association with certain xenogeneic and synthetic bone substitute materials lags behind compared to autogenous bone but steadily increases over time.26 In the present study, the bone densities for groups 1 and 2 were virtually identical (28.74% versus 28.59%), suggesting that, concerning new bone formation, there was no additional beneficial effect of the PRF membrane over the BioGide membrane.

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266 Compared to deproteinized bovine bone mineral (DBBM; Bio-Oss) and biphasic calcium phosphate (BCP; Straumann BoneCeramic), both being widely used for sinus floor elevation in humans, the percentages of bone density, residual filler material, and soft tissue found in the present study are very similar.9,10 However, in the study by Cordaro et al,9 bone density measurements closer to the residual bone of the ridge were higher (23.5% for DDBM and 27.8% for BCP) than those over the whole augmented region (19.8% for DBBM and 21.6% for BCP). The 28.7% new bone found in the present study, which corresponds to the whole augmented region, may thus be regarded as a relatively high bone density value. Another study by Artzi et al,20 where a 1:1 mixture of BCP and autogenous bone was used for sinus floor elevation, showed the same bone density after 6 months (28.6%) as in the present study (28.7%), underlining the efficacy of this synthetic bone substitute material. Taken together, the available histologic and morphometric data in humans suggest that the amount of new bone formed after augmentation with a synthetic hydroxyapatite-silica gel is at least as good as with many other bone substitute materials and that this biomaterial is thus of interest and has clinical merit. There are different means of degradation of calcium phosphate-based biomaterials, including resorption by osteoclast-like cells, chemical dissolution, and phagocytosis of very small par-

ticles by macrophages.30 The fact that tartrate resistant acid phosphatase (TRAP)-positive cells were observed on the nanocrystalline hydroxyapatite suggests that osteoclast-like cells are involved in the degradation process.31 Although the major focus of the present investigation was on the histomorphometric analysis, a short histologic description of the soft tissue component and the biomaterial– soft tissue interface was also given. Numerous large multinucleated giant cells were observed mainly on the biomaterial surface not covered by new bone. These cells resembled osteoclasts. However, their size and number of nuclei and the expression of TRAP are not sufficient to characterize these cells as being osteoclasts. A definitive characterization of these multinucleated cells requires a combined effort of immunohistochemistry and transmission electron microscopy and will be the subject of a separate publication. Since most biomaterials are not inert, they exert influence on the resident cells (fibroblasts, inflammatory cells) as long as they are present. This in turn likely influences the long-term outcome of bone marrow development, filler degradation, and bone formation/resorption.

Conclusion This study showed that the nanoporous hydroxyapatite-silica gel used for sinus floor elevation in humans is osteconductive, supports new bone formation comparable to

most other bone substitute materials, and appears to undergo degradation mediated at least in part by osteoclast-like cells. Nevertheless, prospective studies with larger patient groups are needed to confirm the present data and also to evaluate the long-term performance of dental implants inserted in areas augmented with nanoporous hydroxyapatite-silica gel.

Acknowledgments The authors are indebted to Mrs M. Aeberhard for her excellent technical assistance. The authors reported no conflicts of interest related to this study.

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Maxillary sinus grafting with a synthetic, nanocrystalline hydroxyapatite-silica gel in humans: histologic and histomorphometric results.

The aim of this study was to evaluate in humans the amount of new bone after sinus floor elevation with a synthetic bone substitute material consistin...
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