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The clinical, histological and histomorphometrical evaluation of decalcified freeze-dries bone allogenic graft (DFDBA) with plasma rich growth factor (PRGF) for alveolar ridge preservation.

INTRODUCTION

Nowadays the dental implant is the most frequent treatment modality to recover the function of the edentulous jaw [1]. The volume and density of the alveolus is crucial in implant site [2, 3]. Healing of extraction sockets is usually associated with the loss of residual ridge height and width.It is hard to place an implant in area with significant bone resorbtion. Post extraction preservation of the alveolar ridge allows to place an implant with suitable esthetic and functional criteria [4-8]. Alveolar ridge resorbtion following tooth extraction may result in 40% to 60% loss of bone height and width within 2 to 3 years. Boneresorbtion may result from anatomic, prosthetic, metabolic, and functional factors [9]. Misch et al speculated that the loss of alveolar ridge bone height and labial plate after tooth extraction is due in part to the constriction of the blood clot within the alveolus and the thin labial cortical plates remodeling in response to impaired blood supply after the extraction [10]. The use of bone substitute and GBR techniques have been shown to enhance socket healing and to reduce the resorbtion process. Alveolar ridge augmentation procedures are frequently used to increase ridge height and width prior to dental implant placement. Currently there are some case reports of ridge augmentation results. The results showed the positive treatment effects [11].

Site preservation following tooth extraction through bone grafting helps to reduce the dimensioneschanges thereby reducing resorbtionof vertical bone height and prevention of collapse soft tissues at the site. This technique is crucial to obtain optimal esthetic and functional restoration results. Generally implant placement in a healed socket has got a higher degree of predictability and stabilization soft tissue contour 8.Studies have shown the beneficial effects of the use of regenerative biomaterials in augmenting the alveolus following extractions including autogenous, allogenic, xenograft, and alloplast sources [12, 13]. Nowadays, allograft materials have a major role in bone repair due to the success in space maintenance, rapid bone turnover, biocompatibility, and no need to harvest from another site [12-19]. Demineralized bone matrix (DBM) is a biomaterial which is a production of Iranian Tissue Bank Research and Preparation Centre Imam Khomeini Medical Complex, Tehran, Iran. Preparation of demineralized bone matrix Human long bone shafts were acquired with aseptic techniques from cadaver, routine microbial and viral tests were accomplished according to FDA and AATB protocols. The cortical shafts and cancellous part were debrided, stripped off periosteum, and treated to remove lipid, blood, and cellular remnants before being frozen to -70 C and segmented. The bone segments were immersed in an ethanol and then ethyl ether to cover the tissue. They were rinsed with water and sent to mixing with ethanol. Then, it was mixed with HCL. Next, it was rinsed with PBS until reached pH 7-7.4. Finally, the resulting powder was lyophilized, packed and sent for irradiation with 25 KGy gamma rays [20, 21].

In a study performed by Khoshzaban et al. in 2011, three demineralized bone-matrix allograft materials including ITB, p TCP, Bio - OSS on inflammation and bone formation in defects made in mice calvaria are compared, and the highest bone formation occurred in ITB-DBM group [20]. The use of biologically active endogenous proteins for regenerative purposes, has performed a new way for tissue regeneration. In 1999, Anitua [22] described a new method to prepare platelet-rich plasma called PRGF. This is a 100% autologous procedure which is rich in biologic mediators to accelerate hard and soft tissue regeneration. Adhesive molecules derived from plasma, such as fibrinogen, fibronectin, vitronectin, and thrombospondin-1 act as matrix or scaffold and absorb platelets and stem cells. Platelets are rich source of growth factors including PDGF, TGFB, VEGF, FGF, insulin like growth factor (IGF) and GM-CSF [22-24] .Plasma rich in growth factor (PRGF) is an autogenous plasma product which releases some growth factors and bioactive proteins following calcium activation, and accelerates wound healing and tissue regeneration process [22]. Plasma rich in growth factor is derived from the patient's own blood using simple methods, and is promptly used in surgery location after preparation. Since PRGF contains high concentration of growth factor, can cause accelerate or increase regeneration [26]. In a research done by Behniaet al. (2012), histologic evaluation of the effect of DBM with Mesenchymal stem cells and PRGF on bone regeneration, the results showed that PRGF and MSCs had positive treatment effects [25].

In another research which done by Anitua et al [24]. for evaluating the effect of PRGF in combination with allograft materials on osteo-regeneration, showed that plasma rich in growth factors improves the condition required for osteo-regeneration in implant installation site. So this study was aimed to compare DFDBA alone with DFDBA inconjunction with PRGF in socket preservation clinically, histologically and histomorphometrically.

MATERIALS AND METHODS

Case selection:

In this experimental, randomized, controlled clinical trialstudy,10 subjects with a non-restorable tooth requiring extraction which candidates for the socket preservation and subsequent implant replacement in mandibular jaw were selected. After ethical approvement, ten dental sockets were divided in two groups including test group and control group. DFDBA with PRGF and absorbable membrane collagen for test group, and merely DFDBA and absorbable membrane collagen for control group were used, and the effect of PRGF was evaluated. Patients were chosen that were being healthy; non smoker patients; had good cooperation; were available for follow up courses, and accepted their cooperation on this project in written. Patients with debilitating systemic diseases or diseases that have a clinically significant effect on the periodontium (ex. un controlled diabetic disease ,immune disease ,...); history of oral anticouagulant ,immune suppressor drug and intravenous bisphosphonate use or oral bisphosphonate use for >3 years; pregnancy; known allergy to any material used in the study; heavy smokers; previous head and neck radiation therapy; chemotherapy in the last 12 months; severe psychologic problems; poor oral hygiene; or had not good cooperation were excluded.

Clinical and Radiographic Parameters:

Prior the surgical procedure, each patient received a standardized periapical radiographs clinical photographs at baseline and after 3 months. occlusal stents were fabricated on the study casts to serve as fixed reference guides for the vertical measurements. Vertical distance were measured mesial, distal, mid buccal, and lingual surfaces using a 15-mm periodontal probe immediately after extraction. The same guide was used at the implant placement time to measure the amount of vertical dimension changes at the same four sites from. All clinical measurements were recorded by the same examiner. The difference in the measurements for all surgical sites at baseline and at 3 months, provided a clinical evaluation of the amount of bone resorbtion. Prior to implant placement bone core samples were retrieved from the center of the healed socket for histologic and histomorphometric.

PRGF preparation:

To PRGF preparation, at least 20-milliliter arterial blood was taken and the samples were preserved in sterile blood collecting tubes containing half a milliliter anticoagulant agent (sodium citrate 3.8%). Based on technical standards (PRGF), blood sample was initially centrifuged for eight minutes at 460g velocity. The blood segregates into four parts, the higher part of the tube (1ml) is plasma poor in growth factors (PPGF), then (0.5 ml) plasma growth factors (PGF), Plasma rich in growth factors (PRGF) immediately (0.05 ml) above white blood cells (WBC) and red blood cells (RBC). For this study, PRGF was used. PRGF was taken by half a milliliter pipettes and transferred to a separate tube and was used for soaking allograft material.

Surgical Procedure for Test Group:

Patients received prophylactic antibiotics and 0.12% chlorhexidinerinses 30 minutes prior to surgical procedures. Following administration of local anesthesia, the extraction was carried out atraumatically (with flapless technique and separation of periodontal ligaments around the teeth and carefully luxation using periotomes). The socket was debrided to remove all remnants of the periodontal ligament and inflamed tissues. Socket walls were measured by using guide at four sites and recorded. DFDBA with PRGF was mixed and lightly packed into the extraction socket with a flat plastic instrument. The site was covered with resorbable collagen membrane to prevent the collapse of the surrounding soft tissue into the socket during the healing process and was secured using a reverse cross-mattress resorbable suture. Post-operative care comprised of 0.12% chlorhexidine rinses twice daily for 4 weeks, systemic antibiotic(amoxicillin 500 mg every 8 hourly) for 1 week, analgesic medication (Ibuprofen 400 mg every 8 hours) for 3 days. After 3 months clinical evaluation was performed and a Panaromic and CBCT radiograph from the site was taken. Following local anesthesia fullthickness flap was reflected .Clinical measurement was made using the same guide used previously at baseline at the same four sites to recorded bone-wall height. A small core of newly formatted bone was removed from the center areas of the sockets using a trephine (3-mm-outside-diameter,2-mm-inside-diameter) with irrigation at a bur speed of 1,000 rpm. The samples had been collected and placed immediately in 10% buffered formalin. A dental implant was placed in the socket subsequent to performing a complete osteotomy according to the recommendations of the manufacturer. Healing abutments or cover screws were placed based on primary stability of the implant, and flaps were secured with 4-0 PGA sutures.

Surgical protocol for the control group patients was followed exactly as for the test group except that the extraction socket was received DFDBA alone with resorbable collagen membrane (Fig. 1).

Histologic and Histomorphometric evaluation:

The biopsies taken from human jaws were transferred to 10% formalin solution and kept for at least ten days for complete fixation. Then those were transferred to 10% formic acid solution and kept for one week in that solution. In this period they were inspected in a daily basis to control decalcification. After that, samples were taken off the formic acid solution and were soaked for five minutes in 20% lithium bicarbonate solution to neutralize acid. Each sample was marked with a number. Finally, bone samples were cut vertically two halfes. Central part of the bone was marked by Indian INK. The samples were placed in paraffin blocks. Five micron slides were gotten from paraffined blokes and were stained by hematoxylin-eosin method. Then the microscopic slides were evaluated histopathologicaly and histomorphometricaly by an oral pathologist using Olympus BX41 light microscopic. In histopathologic study grade of inflammation, bone trabecular thickness, type of bonebiomaterial connection (existence or absence of connective tissue between bone parts), area of bone formation and number of blood vessels were evaluated. It is worth to mention that the numbers of blood vessels are evaluated in three scopes at 40x zoom level, and scored as [26]:

Less than three blood vessels considered as 'zero', between three and five blood vessels were 'one' and more than five blood vessels considered as 'two'.

Grade of inflammation in five grades was evaluated [27]:

Grade 0: Absence of inflammatory cells

Grade 1: Little and scattered inflammatory cells (slight)

Grade 2: Five to ten inflammatory cells (focal)

Grade 3: Eleven to fifty inflammatory cells (Focal)

Grade 4: More than fifty inflammatory cells (severe inflammation)

For histomorphometric Evaluation, photographs were taken from all sections taken from grafted area by camera, Olympus DP12, Tokyo, Japane and attached to light Olympus microscope at 40x magnification. The

images were assesd by SIS LS Starter software in Jpeg format. Then area of bone formation were measured and percentage of bone formation to total area of the image were calculated.

Also bone trabecular thickness was measured, including three grades 27:

Grade I: More than 60 microns (Thick)

Grade II: Between 21 to 60 microns (medium)

Grade III: Between 1 to 20 microns (Thin)

To prevent any bias in histologic and histomorphometric interpretation, in none of the steps the pathologist was aware of biopsy content. To precise assessment of measures in this method, seven sections were selected from each biopsy, and their mean value eventually reported as definite result.

RESULTS AND DISCUSSION

Data Analysis:

In this study, data were analyzed using SPSS software, version 18.8. Clinical values in first and second surgical steps were statistically evaluated using Mann-Whitney U test and T test. P<0.05 was considered significant.

Results:

Clinical Findings:

There was no statistically significant difference in vertical bone resorbtion for either study groups. Three months later, the extraction site was healed without any adverse event and free of infection or symptoms in both groups; also complete soft-tissue closure was present 14 days after extraction. Membrane exposure did not compromise the early stage of soft-tissue healing.

histomorphometric analysis:

The results indicated that there was a statistically significant difference between the two groups based on :area vital bone regeneration which was 62.5% [+ or -] 3.2% in test group compared to 31.7% [+ or -] 1.1% control group(P = 0.000). trabecular thickening more in test group incompare with control group(48.08 [+ or -] 10.37, 28.22 [+ or -] 2.83 [micro] respectively) (P=0.003) and residual biomaterial in test group compared to control group were respectively(0/03% , 0/08%) (P=0.03). Histomorphometric analysis is summarized in Table1.

Histologic findings:

Control group

blood     bone-biomaterial   Vitality **   foreign
vessels      contact *                       body
score                                      reaction
                                             ***

1                +                +           -
1                +                +           -
2                +                +           -
2                +                +           -
2                +                +           -

Test Group

blood     bone-biomaterial   Vitality **   foreign
vessels      contact *                       body
score                                      reaction
                                             ***

2                +                +           -
2                +                +           -
2                +                +           -
2                +                +           -
2                +                +           -

Control group

blood     inflammatory   Number
vessels   infiltration   of case
score        grade

1              1            1
1              3            2
2              1            3
2              4            4
2              1            5

Test Group

blood     inflammatory   Number
vessels   infiltration   of case
score        grade

2              3            1
2              1            2
2              1            3
2              1            4
2              1            5

* +: Direct contact between bone and biomaterial, Presence of
connective tissue between bone and biomaterial.

** +:Vital bone, -: Non vital bone.

*** +:Presence foreign body reaction -:No foreign body reaction.


Histologic Observations:

Histologic slides in test group were prepared, and examination was performed at *400 magnification to the cores revealed formation of new well-mineralized and vital trabecular bone. The new bone was organized in trabecular,with collagen fibers arranged in a meshwork pattern, osteocytes randomly distributed within the trabecular in large spindle-shaped lacunae. Thin and aboundent blood vessels were observed in the test group. In histologic slides assessmentin control group were observed the trabecular bone with less density and irregularly pattern. Thin and less blood vessel were found.

Discussion:

The results of this study showed that the clinical mean value of vertical ridge analysis in four distinct regions of dental socket in test group was lower than control group, but the difference is not statistically significant. Histomorphometrical mean value of trabecular and area of bone formation percentage was higher in test group compared that control group, and residual biomaterial was lower in test group compared with control group and showed a statistically significant difference. Histologically, mean value of blood vessels was higher in test group than control group. In 20% of slides, the number of blood vessels was grade 1 and in 80% was grade 2. According to these results, no foreign body reaction was found in samples, inflammation was slight, and the bones were vital in all samples. A direct contact between biomaterial and bone was observed in all samples. In histomorphometric studies on microscopic sections, aside from numerous benefits, having a two dimensional image of a three dimensional space puts limitations on studying and analysis of histologic sections of osteogenesis process [29]. Therefore, it can be mentioned that beside the effects of biologic factors on trabecular bone, some technical problems such as producing sections in longitudinal direction of the defect (perpendicular or parallel) are definitely affecting the resulted microscopic image and this can explain the existing difference in study results. On the other hand, reported histomorphometric values should be compared and analyzed with caution, because taking biopsy in animals differs from taking biopsy in human. In addition, taking bone core samples in human studies is done in different ways, some are taken vertically, and some are taken horizontally [30]. In this study trabecular thickness and percent of osteogenesis was higher in test group than control group, which is in accordance with the studies in which growth factors derives for increased bone regeneration from the patient's own blood [31-35].

KutKut et al8. suggested the positive effect of PRP and bone regeneration enhancement. Other similar results conforming to our findings are reported by Kassolis [36], Marx [37] and Anitua [22]. In a study done by Gurbuzer et al, [38] PRGF was used for bone regeneration, and PRGF ineffectiveness was reported. In addition, other similar studiesindicated the ineffectiveness of PRP in bone defects [39, 40], which was in contrary to the results of this research. Some studies indicate that a reason explaining this discrepancy can be various methods in PRGF production, (including system, different concentration of platelet and growth factors, time of application). Also, PRP effect is dose dependent, and is mainly effective in 9 to 6 times concentrations, while the higher concentrations has binding effects [38-43]. Based on the current study, a slight residual biomaterial inflammation is seen in test group compared to control group, which is an indication that allograft material is quickly absorbed and well tolerated. A similar result is observed in KutKut et al. studies8. Therefor this can be an indication that autologous blood-derived growth factors have accelerative role in allograft material absorption and its transformation to bone. According to findings of present study regarding biomaterial contact quality, in all the cases a direct contact and lack of connective tissue is reported which is in contrary to findings of Anitua et al [23]. as they indicated that connective tissue exist between allograft material and bones. Considering vitality of newly formed bones, it seems that allograft material with and without platelet-rich plasma acts as a framework for normal osteogenesis, which is conforming to the results of studies done for autologous bloodderived growth factors [8, 42, 43]. In a study done by Toloue et al. the average residual allograft after application of calcium sulfate with freeze-dried bone allograft material is reported 2.5%, however, in current study the residual allograft is less than this value, which is probably because of absorption accelerative factor of PRGF in grafted region[30]. In this study DFDBA allograft was used as a useful substitute for autogenous allograft in patients with alveolar ridge defects. The results are in accordance with results of studies in which allogeneic bone material is used for augmentation of ridge defects and alveolar ridge preservation [12-18]. Since autograft causes unwanted surgery traumato other parts of the body, there is no doubt that, a suitable substitute with similar character that eliminates the need for allograft removal surgery will be beneficiary to both patient and physician19. DFDBA is as osteoinductive allograft but FDBA is considered an osteoconductive allograft, however, based on laboratory researches, DFDBA has a higher potential for osteogenesis than FDBA. This will significantly increase vital bones compared to FDBA, therefore it is considered a preferred method, which is in accordance with studies in which DFDBA is used as bone allograft material for alveolar ridge regeneration [28, 13, 14].

The material used as barrier membrane in GBR should have properties such as tissue compliance, tissue integration, preventing invasion of adjacent host tissue cells, and simple clinical application. One of the drawbacks of bio-absorbable membranes is limited control over membrane absorption time as it supposed to be capable of maintaining its structural rigidity for a period time of over six months while it promptly undergoes decomposition by enzymes derived from macrophages and neutrophils and loses its rigidity [44]. In current study, a pericardium absorbable allogeneic membrane with 0.2 to 0.6 mm thickness was used, therefore it advisable to perform a similar study using non-absorbable membrane to ensure that soft tissue is ineffective in guided osteo-regeneration process. One of the advantages of the current study is its humanistic nature that enables its finding to be generalized for other human samples.

Conclusion:

Based on the results of the study, the histomorphometric findings suggest that PRGF enhanced bone regeneration more than PRGF-free graft. Although no clinical and histological difference were found.

ARTICLE INFO

Article history:

Received 21 September 2014

Received in revised form 25 November 2014

Accepted 22 December 2014

Available online 3 January 2015

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(1) Niloofar Jenabian, (2) Aisenpouri, (3) Maryam seidmajidi, (1) Ali Bijani

(1) Associate professor, Department of periodontology

(2) Assistant Professor, Department of periodontology

(3) Associate professor, Department of pathology

Corresponding Author: Niloofar Jenabian, Associate professor, Department of periodontology

Table 1. Histomorphometric Analysis.

                               Test group            Control group
                             mean [+ or -] SD       mean [+ or -] SD

Trabecullar thickening     48.08 [+ or -] 10.37   28.22 [+ or -] 2.83
Area of bone formation %   0.62% [+ or -] 0.03    0.31% [+ or -] 0.011
Residualbiomaterial        0.03% [+ or -] 0.020   0.08% [+ or -] 0.45

                           P-value

Trabecullar thickening      0.003
Area of bone formation %    0.000
Residualbiomaterial         0.03

Fig. 1: The average vertical bone loss in test and
control group are summarized.

Error bars: 95% Cl

          Control   PRGF

Mesial    1.6       1.0
Distal    0.8       0.6
Buccal    1.6       0.8
Lingual   1.4       0.8

Note: Table made from bar graph.
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Author:Jenabian, Niloofar; Aisenpouri; seidmajidi, Maryam; Bijani, Ali
Publication:Advances in Environmental Biology
Article Type:Report
Date:Nov 1, 2014
Words:4911
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