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   Table of Contents    
Year : 2014  |  Volume : 18  |  Issue : 2  |  Page : 213-219  

Comparison of nanocrystalline hydroxyapatite and synthetic resorbable hydroxyapatite graft in the treatment of intrabony defects: A clinical and radiographic study

1 Department of Periodontics, Institute of Dental Studies and Technologies, Kadrabad, Modinagar, Ghaziabad, Uttar Pradesh, India
2 Department of Periodontics, Subharti Dental College, Meerut, Uttar Pradesh, India

Date of Submission23-Aug-2013
Date of Acceptance28-Oct-2013
Date of Web Publication23-Apr-2014

Correspondence Address:
Mansi Bansal
Shant 196 A Saket, Meerut - 250 003, Uttar Pradesh
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0972-124X.131329

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Background: The aim of this study is to compare, clinically and radiographically, the effectiveness of nanocrystalline hydroxyapatite (NHA) and synthetic resorbable hydroxyapatite (HA) in the treatment of intrabony defects. Materials and Methods: Ten subjects with bilateral defects, with probing depth (PD) 6-9 mm and radiographic evidence of an intraosseous component ≥4 mm participated in the present study. Subjects were allocated randomly to treatment with NHA (test group) or HA (control group). At baseline, 3 and 6 months after surgery, the following clinical parameters were recorded: Plaque index, gingival index, PD, relative attachment level (RAL), and radiographic reduction in intrabony defect. Results: At 6 months following therapy, the test group showed a reduction in mean PD from 6.4 ± 0.843 to 3.3 ± 0.8232 mm and a change in mean RAL from 12.9 ± 1.197 to 10.1 ± 0.7378 mm, whereas in the control group the mean PD decreased from 7.65 ± 1.8566 to 3.9 ± 1.1005 mm, and mean RAL decreased from 13.9 ± 0.9944 to 10.7 ± 0.6749 mm. On comparison of the mean difference in probing depth between the two groups after the unpaired t-test was applied at baseline, 3 months and 6 months, scores were found to be statistically non-significant (P > 0.01). Conclusion: The results of the present study indicate that both NHA and conventional HA led to the improvement of clinical and radiographic parameters over the course of the study. However, the test group did not show any significant improvement over the control group.

Keywords: Chronic periodontitis, debridement, hydoxyapatite, nanocrystalline, regeneration

How to cite this article:
Bansal M, Kaushik M, Khattak BB, Sharma A. Comparison of nanocrystalline hydroxyapatite and synthetic resorbable hydroxyapatite graft in the treatment of intrabony defects: A clinical and radiographic study. J Indian Soc Periodontol 2014;18:213-9

How to cite this URL:
Bansal M, Kaushik M, Khattak BB, Sharma A. Comparison of nanocrystalline hydroxyapatite and synthetic resorbable hydroxyapatite graft in the treatment of intrabony defects: A clinical and radiographic study. J Indian Soc Periodontol [serial online] 2014 [cited 2022 May 21];18:213-9. Available from:

   Introduction Top

The shift in therapeutic concepts from resection to regeneration has significantly impacted the practice of periodontology in last quarter of the century. [1] The key to tissue regeneration is to stimulate a cascade of healing events which, if coordinated, can result in completion of integrated tissue formation. [2] Although the achievement of the goal of complete regeneration of the periodontal tissues may not be possible for many years, recent developments in nanomaterials and nanotechnology have provided a promising insight into the commercial applications of nanomaterials in the management of periodontal diseases e.g., nanocrystalline hydroxyapatite (NHA) paste (Ostim, Heraeus Kulzer, Hanau, Germany) containing 65% water and 35% nanostructured apatite particles has widely been used for augmentation procedures in osseous defects. [3]

Nanomaterials have significant surface effects, size effects, quantum effects, and exhibit much better performance properties than traditional materials. [4] Another important feature of nanostructured materials is the development of self assembly. Here, an autonomous organization of components into patterns or structures occurs without human intervention. [5]

Another form of synthetic NHA is obtained from chemical precipitation using aqueous solution of calcium nitrate tetrahydrate and ammonium dihydrogen phosphate by hydrothermal treatment. [6] Advantages of this material are the close contact with surrounding tissues, quick resorption characteristics and large number of molecules on the surface. [3],[7] Nanophase HA also can promote proliferation and osteogenic differentiation of periodontal ligament cells and further it may be used as a bioresorbable agent in osseous restoration. [8]

Therefore, in view of various positive effects of NHA in bone regeneration the current study was designed to clinically and radiographically evaluate the efficacy of NHA and synthetic resorbable HA graft in the treatment of intrabony defects.

   Materials and Methods Top

A clinical and radiographic study was carried out to assess the efficacy of treatment of human intrabony defects with NHA (particle size: ~20 nm) (Group A) and with conventional HA (particle size: 15-35 × 10 4 nm) (Group B) in the treatment of human intrabony defects. Patients were selected from Out Patient Department (OPD) of Periodontics.

Ten patients (8 males and 2 females) aged between 20 and 50 years with moderate to advanced chronic periodontitis with bilateral clinical and radiographic evidence of angular defects were recruited for the study.

Inclusion criteria

  1. Moderate to severe periodontitis, diagnosed on the basis of bleeding on probing, probing depth, and clinical attachment loss
  2. Patients having pocket depth of 6-9 mm
  3. Patients with vertical intrabony component of ≥4mm.

Exclusion criteria

  1. Any systemic disease that might affect the periodontium
  2. Any recent periodontal surgery within 6 months
  3. Smoking
  4. Uncooperative patients.

The patients selected on the above criteria were then explained about the treatment procedure and the associated risks and benefits and their written consent was obtained. Four weeks following phase I therapy a periodontal re-evaluation was performed to confirm the suitability of the sites for the study.

The following recordings were made at baseline

  1. Demographic data, medical history, dental history, and personal history
  2. Clinical examination of the dentition
  3. Parameters:
    • Bleeding on probing (Ainamo and Bay) [9]
    • Gingival Index (Loe and Sillness) [10]
    • Plaque index (Sillness and Loe) [11]
    • Oral hygiene Index - S (Greene and Vermillion) [12]
    • Probing depth (PD) and Relative attachment level: An occlusal stent was fabricated for positioning of the periodontal probe {University of North Carolina No. 15 Probe. (Hu-Friedy)}. [13],[14] A wire was placed on the bucco-occlusal line angle of teeth during fabrication of stent. This wire was then exposed by making grooves in the inter-dental regions, such that the probe when inserted in the inter-proximal area was in contact with the wire; hence, the probe position and angulation remained the same for all pre and post operative measurements. Using the groove and wire as a guide, the periodontal probe was inserted into the gingival sulcus and PD (using the gingival margin as reference), and relative attachment level (using the stent wire as reference) was recorded
    • Digital Radiography: Radiographs were taken using the RINN XCP system ® (Dentsply, USA) by the standardized paralleling technique with the digital radiovisiography (RVG) (Suni Ray ® Suni Imaging Micro system Inc.) at baseline, 3 months and 6 months post-operatively. The size of the defect was calculated using the RVG software X-ray Vision ® Apetryx. The infrabony component was assessed by identifying the parameters and calculated as stated by Eickholz. [15]

All radiographic measurements were made to the nearest 0.01 mm.

Preparation of nanocrystalline hydroxyapatite

The experimental material was synthesized and characterized at Smart Materials Research Laboratory, Department of Physics, IIT Roorkee, India.

0.5M Ca (NO 3 ).24H 2 O (Merck) in ethanol with a pH 10.5 was added to 0.5M ammonium phosphate [(NH 4 ) 2 PO 4 ](Merck) slowly at a rate of 8ml/min and at constant temperature (80 ° C) with vigorous stirring. The resultant sol-gel was continuously stirred at a constant pH of 10 was kept constant by adding Ca (OH) 2 solution and a constant temperature of 70°C for 5 hours. After allowing the product to cool, it was kept inside the oven at 50°C overnight. The product was sintered for 3 hours at 350°C.

The formation and quality of the synthesized compound as prepared and heat treated at 350 0 C for 2.5 was studied using an X-ray diffractometer (XRD) (Pw1140/90), using Cu Kα(λ=0.15418 nm) in a wide range of Bragg angles (10°-2θ-70°) at room temperature.

Scanning electron micrographs were obtained with scanning electron microscope (SEM) LEO VP STEREOSCAN. Elemental analysis of the synthesized powder was determined by energy dispersive x-ray analysis (EDAX) attached with the SEM.

Determination of Ca/P ratio

The stochiometric (Ca/P) ratio of the as synthesized sample was determined by EDAX. It was found that Ca/P ratios nearly coincide with the theoretical value (1.67) of HA.

X-ray diffraction patterns

X-ray crystallography is a method of determining the arrangement of atoms within a crystal, in which a beam of X-rays strikes a crystal and diffracts into many specific directions. X-ray diffraction techniques play an important role in the analysis of crystallite sizes. The patterns due to the as-prepared material bear with it the characteristic patterns of HA but not with much resolution and intensity. It contained no other crystalline phase other than HA. The broad patterns around at 30° indicate that the crystallites are very tiny (~20 nm) in nature with much atomic oscillations. Here the mother liquor is expected to permit selective growth of multitudes of HA crystallites with high rate thus avoiding orderly growth of large crystals.

The XRD patterns of the heat treated material at 350°C show an increase in intensity of the diffraction peaks. Again it rules out the formation of any new crystalline phase other than HA.

Scanning electron microscopy

Analysis of micrographs reveals nanometer size of the powder confirming the XRD analysis. There are many spherical agglomerations and crystallites of submicrometric in size with a tendency to agglomerate leaving submicrometric pores in between.

Surgical procedure

Local anesthesia (2% lidocaine, epinephrine 1: 100,000) was injected in the site of surgery. Crevicular incision was given in the sextent of the defect and a mucoperiosteal flap was raised. The area was degranulated, curetted, and irrigation was done with diluted betadine solution. Defect was isolated and the graft (NHA or HA) was wetted in patient's own blood and placed in small increments in the defect using an amalgam carrier and condensed until the defect was filled. The sutures were then tightened over the defect site and also placed in the adjacent sites so as to ensure complete approximation of the flaps. Direct loop sutures were given over the site of the defect. Following this a periodontal pack was applied over the site [Figure 1] and [Figure 2].
Figure 1: (a) Periapical radiograph showing vertical defect mesial to tooth #46. (b) Preoperative view of probing depth. (c) Clinical view of the intrabony defect after debridement

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Figure 2: (a) NHA powder in place prior to suturing. (b) Six-month periapical radiograph. (c) Healing at 6 month postoperatively

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Statistical analysis

The data regarding the clinical and radiographic parameters was tabulated and subjected to statistical analysis. Student's paired t-test was used to compare data from baseline to that of 3 months and from baseline to 6 months for each treatment group. Comparison between the test and the control group (intergroup) at baseline 3 months and 6 months were accomplished using Student's unpaired t-test.

   Results Top

Twenty subjects (N = 10 in each group) completed the 6-month follow-up period. In all treated sites, primary closure was obtained at completion of the surgical procedure. The postoperative healing was uneventful in all cases. No complications or infections were observed throughout the study period. Radiographs and clinical photographs for NHA and HA are shown in [Figure 1] and [Figure 2]. The mean and standard deviation scores at baseline, 3 months, and 6 months for test and control groups are summarized in [Table 1]. No statistically significant differences were found between the groups for any of the investigated parameters at baseline. Intra group comparison by means of paired T test from baseline to 3 months and from baseline to 6 months and from 3 to 6 months for each treatment group is summarized in [Table 2].
Table 1: Mean±SD scores at baseline, 3 months, and 6 months (N=10 subjects in each group) for test and control groups

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Table 2: Paired T test data from baseline to that of 3 months and from baseline to 6 months and from 3 to 6 months for each treatment group

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Following treatment, PI values remained low throughout the study period in both groups.

On comparison of the mean difference in PD between the two groups at baseline, 3 months and 6 months, scores were found to be statistically insignificant (P > 0.01), as the calculated t values at baseline, 3 months, and 6 months were 1.9384, 0.88465, and 1.38054 (T TAB ≈ 2.88) [Table 3].
Table 3: Unpaired t test data from baseline to that of 3 months and from baseline to 6 months and from 3 to 6 months for each treatment group

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On comparison of the mean difference in relative attachment level between the two groups after the unpaired t test was applied at baseline, 3 months, and 6 months, scores were found to be statistically non-significant (P > 0.01), as the calculated

t values at baseline, 3 months, and 6 months were 2.031, 1.878, and 1.897 (T TAB ≈ 2.88) [Table 3].

On comparison of the mean difference in radiographic measurements between the two groups after the unpaired t test was applied at baseline, 3 months, and 6 months, scores were found to be statistically non-significant (P > 0.01), as the calculated t values at baseline, 3 months, and 6 months were 0.17, 0.46, and 0.2410 (T TAB ≈ 2.88) [Table 3].

   Discussion Top

Conventional HA graft (Periobone G), a bioceramic resorbable alloplast, with a particle size of 150-250 μ used in the current study served as a control group. The results of the present study demonstrated an improvement in clinical and radiographic parameters with use of HA graft. The difference in the oral hygiene status from baseline to 3 months and 6 months respectively and from 3 months to 6 months were statistically insignificant. This suggests that oral hygiene was maintained optimally well throughout the period of study. Similar pattern was observed for the plaque scores and gingival index scores. Yukna et al. [16] and Meffert et al. [17] also reported no effect on the plaque index when HA graft was used in treatment of intrabony defects. The above studies, like the present followed strict plaque control and maintenance of oral hygiene throughout the study period. These observations suggest that HA was well tolerated in the hard and soft tissues and does not seem to evoke any inflammatory response significantly. The similar results have been confirmed clinically by Kenny et al. [18] who reported uneventful post-operative healing. The HA was well tolerated by the gingival tissues during initial healing and thereafter including 6-month evaluation period.

The present study demonstrates a decrease in PD from baseline to 3 months and 6 months with difference of 3.25 ± 1.2304 mm and 3.75 ± 1.6874 mm respectively which was found to be statistically significant. However, the decrease from 3 to 6 months was statistically insignificant. Similar observations were seen for relative attachment level. These findings signify the use of HA graft in the clinical resolution of intrabony defects. Also, Kenny et al. reported in the re-entry data that there was a measurable improvement in the gain of attachment level which was duplicated with an equivalent improvement in the depth of the defect seen at re-entry.

In accordance with the observations of the current study, Yukna et al. [16] also reported a decrease in pocket depth of 2.8 ± 1.4 mm and gain in clinical attachment level of 1 ± 0.1 mm. On comparison with the current study, this decrease is less. This is because the period of evaluation in the study of Yukna et al. was of 5 years during which some recurrence might have occurred due to the lack of oral hygiene maintenance by the patients.

The improvement in the clinical probing and relative attachment level was well supported by the decrease in the radiographic area of the intrabony defect in the control group of the present study, which was determined in a manner similar to that as described by Eickholz et al. [19] The observations of the present study show a decrease in the size of the defect from baseline to 3 and 6 months respectively to be statistically significant. Also, the difference from 3 months to 6 months was statistically significant.

The increase in the radiodensity in the defect, and hence a decrease in the defect size, signifies that use of HA graft results in resolution of the intrabony defect. However, the nature of the restoration of the defect that whether the graft acted as a filler material or allowed for ingrowth of the bone cannot be inferred from the clinical and radiographic observations of the present study. Evaluation of the true nature of attachment requires histological investigation.

In accordance with the radiological observations of the current study, Okuda et al. [20] and Scabbia et al. [21] evaluated the depth of the intrabony defect radiographically using the same landmarks used in the current study after a period of 12 months and reported significant gain in the bone height and reduction of the depth of the defect.

Osteoconductivity, solubility, sinterability, and mechanical reliability of HA can be enhanced by controlling its particle size and structural morphology in the order of a nanoscale. NHA which has been used as a test material in the present study posseses exceptional biocompatibility and bioactivity properties with respect to bone cells and tissues, probably due to its similarity with the hard tissues of the body.

Beside a good biocompatibility, a synthetic bone substitute should also ensure the formation of new bone after their implantation. It would seem rational to suggest that particles too large in size will resorb at a slower rate and offer a overall reduced surface area, while particles too small in size may induce inflammation, be readily resorbed or phagocytosed and result in an interparticulate space of a reduced dimension that would not be conducive to cellular migration and ingrowth. [1] In fact, an optimal synthetic bone substitute is resorbed by hydrolytic and cellular degradation process involving the action of macrophages and further is replaced by vital bone over time. A major prerequisite for this process is angiogenesis because newly formed blood vessels transport oxygen and nutrients into the implanted bone substitute, a physiological milieu is created, which supports the ingrowth of bone cells and also differentiation of pluripotent stem cells from the surrounding tissue to an osteoblastic phenotype.

Laschke et al. [22] reported that NHA revealed areas of degradation at day 14 after implantation. However, 2 weeks is too early a rate of resorption and clinical results following and any gain in clinical attachment level or decrease in an intrabony defect is highly unexpected. In contrast, our study showed a significant decrease in pocket PD and decrease in radiographic area of defect. Therefore, more histological studies are required to determine the degradation rate of NHA. Furthur Laschke also reported that within these areas, vascularized granulation tissue could directly invade the biomaterial. This guided vascularization may accelerate formation of new bone in bone defects, because osteoblasts are facilitated to migrate into these vascularized areas where the remaining nondegraded fragments serve as scaffold for invading cells. In this process, the newly developing blood vessels play an important role, because it has previously been reported that endothelial cells stimulate the differentiation of preosteoblasts to osteoblasts by expression of osteotropic growth factors, such as endothelin-1 and Insulin like growth factor (IGF -1). Vice-versa, the expression of vascular endothelial growth factor (VEGF) by osteoblasts further sustains the proliferation of endothelial cells and thus the formation of new blood vessels.

Sun et al. [23] in an in vitro study demonstrated that NHA can promote periodontal ligament fibroblast proliferation and osteogenic differentiation in comparison with dense HA. Furthermore, they reported that the increased proliferation capability of periodontal ligament fibroblasts under the influence of nanometer order HA indicated that latter had better compatibility and resorbability than dense HA. Recent research has shown that synthetic nanostructured HA has higher biocompatibility for microvascular endothelium.

Nanostructured HA promotes up-regulation of Fibroblast Growth Factor (FGF)-2 and primes endothelial cells to VEGF action. FGF-2 plays a biological pleiotropic role, including cell migration, angiogenesis, bone development and repair. Also, a synthetic bone substitute must not only support the growth and foster the phenotype of the cell type for the tissue it is to replace (i.e., osteoblasts), but also support the cells that are responsible for maintaining the bone cells (i.e., fibroblasts) The upregulation of FGF-2 through gene transcription is an important event which explains the role of HA nanocrystals in inducing a positive and controlled angiogenic phenotype in endothelium. The robust increase of FGF-2m RNA (3-6 fold) translates into a significant production of the soluble FGF-2 isoform. [24]

In the current study it was decided to use powder form of NHA which served as the test group of the study. The results of the test group demonstrate statistically insignificant difference in plaque scores from 3 to 6 months. A similar trend was seen in the simplified oral hygiene index scores and gingival index scores. On comparison of the test group with the control no significant difference was observed, which showed that NHA did not have any adjunctive effect in improving the plaque scores or the oral hygiene of the patient. These factors were more influenced by the fact that bilateral defects were chosen and patient's own maintenance which was reinforced timely during the recall periods.

In the present study there was statistically significant difference in the PD and relative attachment level between baseline and 3 months and baseline and 6 months in the test group. But there was no significant difference between 3 months and 6 months in the test group. Similar to the other parameters, no significant improvement of the test group was seen over the control group. These observations parallel that of the study of Kasaj et al. [25] who reported significant improvement in PD and clinical attachment level (CAL) at 6 months after surgery compared to baseline. In a previous study evaluating the healing of intrabony peri-implantitis defects following an application of an NHA paste as a graft or a bovine derived Xenograft in combination with a collagen membrane, both treatment procedures produced clinically significant PD reductions and CAL gains.

The use of NHA in the treatment of periodontal defects was evaluated in the pioneer study of Zuev et al. [26] who found Ostim to be not inferior to bone transplant and devoid of its shortcomings in the treatment of 395 patients with periodontal defects including mainly periodontal abcesses. Later Kasaj et al. [25] stated that at 6 months after surgery, the treatment of intrabony periodontal defects with an NHA paste produced clinically and statistically significant PD reductions and CAL gains compared to open flap debridement alone.

On the other hand Heinz et al. [27] compared clinical outcomes of papilla preservation flap surgery with or without the application of a novel NHA bone graft substitute. They observed that after 6 months statistically significant reduction in probing pocket depths and gain in probing bone levels in the test group. These observations were in accordance to that of the present study. Schnettler et al. [28] found that NHA binds to the bone and stimulates bone healing by stimulation of osteoblast activity.

The current study also demonstrates a statistically significant reduction in area of defect from baseline to 6 months and from 3 to 6 months. However, the decrease in area from baseline to 3 months was statistically insignificant. This might be because of the very small particle size and early resorption within 12 weeks as reported by Thorwarth et al. [29] who used microradiography to assess the mineralization content and degradation of the test material. They stated that the accelerated initial ceramolysis of the material did not hinder the bone healing process which follows the principles of a primary angiogenic reossification. Bone regeneration starts from the borders of the defect and carries on centripedally. The ceramic material functions as an osteoconductive guideline for the growing bone trabeculae. They stated that newly formed bone was discriminated from local bone by lower degree of mineralization, the different architecture of spongiosa and lack of alignment of the trabecular trajectory. The present study coincides with the above study and the clinical findings in the present study also reveal evidence of regeneration after 12 weeks (3 months). However, in the present study microradiographic technique was not used. Also, no additional effect of the test group was noted over the control group.

Similar findings were reported by Klawitter et al. [30] who stated that trabeculae of bone vary in size from 20 to over 100 μm. When a trabecula reaches about 100 μm, it carries its own blood vessels, much in the same way an osteon does via Haversian canal. Compact bone has haversian systems or osteons of between 50 and 250 μm. Thus, to support trabecular bone ingrowth, the pores would need to be at least 40-100 μm, and to support osteonal bone ingrowth, pores of at least 100 μm would appear necessary. Later Hirschorn [31] reported that particle size of about 380 μm in diameter would yield this minimal dimension and particles yielding under 100 μm space dimensions may possess less mineralization potential. Therefore in the present study the tested material i.e., NHA which had a particle size of ~20 nm shows statistically insignificant results over the control group.

In view of above, Fucini et al. [32] found that there was no difference in defect fill between demineralized freeze dried bone allograft particles of 250-500 μm size compared to those of 850-1000 μm. In vitro analysis of the interparticulate space among bone replacement grafts condensed under a uniform standard force showed that autogenous bone harvested low and high speed rotary instruments, freeze dried bone allograft (250-710 μm). Bio-oss (Cancellous and cortical), Osteograf LD, Perioglas and Osteogen yielded a 40-100 μm interparticulate space. Autogenous bone harvested by back action chisels, demineralized freeze dried bone allograft (350-500 μm). Osteograf N (300-700 μm), Biocoral, Biogran, Interpore 200 and Calcitite (40-60 μm) HA granules yielded an interparticulate space that was equal to or greater than 100 μm. [33]

Another important property of nanomaterials which might have played a major role in regeneration in the current study is development of self assembly which helps to integrate different functions into synthetic extracellular matrices. These synthetic extracellular matrices will need to perform functions such as to sustain cell viability and proliferation, allow the establishment of a blood vessel network formation and provide sufficient support to prevent tissue collapse. In recent times, developments in this field have seen the use of pH-induced self-assembly of a peptide-amphiphile to artificially construct a nanostructured fibrous scaffold with the structural features of extracellular matrices. After cross linking, the newly produced fibers are able to direct mineralization of HA to form a composite material in which the crystallographic axes of HA are aligned with the long axes of the fibers. This alignment is similar as that observed in vivo between collagen fibrils and HA crystals in bone. [5]

Despite good clinical results the current study was not subjected to histological analysis. Therefore, confirm evidence of periodontal regeneration cannot be stated. Also, differences in the physiochemical and structural characteristics between NHA and HA used in the past and in the present study may lead to differences in the regenerative/osteoconductive properties. Material properties including porosity, surface geometry, and surface chemistry play a role in determining the osteoconductive capacities of a graft which must be analyzed histologically.

   Conclusion Top

Further studies using more subjects and histologic analysis could clarify the benefits of the new synthetic bone grafting material. In addition, a longer post treatment observation interval may be needed to confirm the stability of clinical outcomes.

   References Top

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