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 Table of Contents  
Year : 2021  |  Volume : 11  |  Issue : 3  |  Page : 300-307

Effect of combining platelet-rich fibrin with synthetic bone graft on the healing of intrabony defects after apicectomy in dogs with periapical pathosis

1 Department of Endodontics, Faculty of Dentistry, Ain Shams University, Cairo, Egypt
2 Department of Surgery, Anesthesiology and Radiology, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt
3 Department of Endodontics, Faculty of Dentistry, Ain Shams University, Cairo;Department of Endodontics, Faculty of Dentistry, Misr International University, Cairo, Egypt

Date of Submission18-Jul-2020
Date of Decision03-Oct-2020
Date of Acceptance03-Oct-2020
Date of Web Publication3-Sep-2021

Correspondence Address:
Prof. Ashraf M Abu-Seida
Department of Surgery, Anesthesiology and Radiology, Faculty of Veterinary Medicine, Cairo University, Giza Square, Giza
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/sej.sej_191_20

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Introduction: An apicectomy is traditionally a surgical endodontic procedure that deals with the local excision of the root tip and periapical pathosis of failed conventional root canal treatment. The proper healing of the intrabony defects plays a crucial role in the success of endodontic surgery. This study evaluates the role of platelet rich fibrin (PRF) in conjunction with synthetic bone graft on the healing of intrabony defects after apicectomy in dogs with induced periapical lesion.
Materials and Methods: Induced periapical pathosis and root canal obturation were carried out in 36 mandibular premolar dogs, teeth, then treated with either apicectomy (Group I) or apicectomy followed by application of PRF and synthetic bone graft (Group II). The periapical healing of both groups was evaluated by radiography and histopathology after 1 month (subgroup A) and 3 months (subgroup B). The periapical bone density, percentage of difference in radiodensity, inflammatory cell count, and percentage of new bone formation were measured. The quantitative data of both groups were statistically analyzed. The P < 0.05 was considered statistically significant.
Results: There were significant differences between both groups in periapical radiodensity, percentage of difference in radiodensity, mean inflammatory cell count, and percentage of new bone formation in both subgroups (P < 0.05). In contrast to Group I, Group II exhibited high significant differences between both subgroups in the mean radiodensity, percentage of difference in radiodensity, and new bone formation (P < 0.001).
Conclusions: Using of PRF in conjuction with the synthetic bone graft enhances the healing of periapical intrabony defects after apicectomy in dogs' teeth.

Keywords: Apicectomy, inflammation, intra bony defect, periapical pathosis, regenerative endodontic

How to cite this article:
Basta DG, Abu-Seida AM, El-Batouty KM, Tawfik HM. Effect of combining platelet-rich fibrin with synthetic bone graft on the healing of intrabony defects after apicectomy in dogs with periapical pathosis. Saudi Endod J 2021;11:300-7

How to cite this URL:
Basta DG, Abu-Seida AM, El-Batouty KM, Tawfik HM. Effect of combining platelet-rich fibrin with synthetic bone graft on the healing of intrabony defects after apicectomy in dogs with periapical pathosis. Saudi Endod J [serial online] 2021 [cited 2022 Nov 30];11:300-7. Available from: https://www.saudiendodj.com/text.asp?2021/11/3/300/325394

  Introduction Top

Periradicular surgery is one of the most important modern endodontic interventions. It is usually indicated for excision of the periapical pathosis. Based on several factors, endodontic surgery results either repair or regeneration of the injured bone, periodontal ligament and cementum. These factors include presence of stem cells, extracellular matrix, and some molecules of adhesion and signelling.[1]

After endodontic surgery, regenerative therapy is highly indicated to obtain an optimum healing of the produced periapical intrabony defect. Bone graft materials have been usually used for filling this bony defect. There are several bone graft materials such as; synthetic resorbable hydroxyapatite (HA),[2] calcium sulphate,[3] autogenous bone,[4] HA granules,[5] nanocrystalline HA,[6] an organic bovine bone,[7] enamel matrix derivative,[8] collagen-apatite nanocomposite,[9] demineralized and decalcified freeze-dried bone allografts.[10],[11] Furthermore, platelet-rich fibrin (PRF) is usually applied as a barrier membrane to achieve guided tissue regeneration (GTR). The PRF is a good biomaterial that enhances the wound healing through its fibrin bandage and growth factors.[12]

The healing of intrabony defects after apicectomy plays a crucial role in the success of endodontic surgery. Therefore, there is a continous need for research on the effect of various materilas on bone healing after apictectomy. The aim of this study was to investigate the role of PRF in conjunction with synthetic bone graft in the healing of the produced intrabony defects after apicectomy in dogs with induced periapical pathosis.

  Materials and Methods Top

This work was approved by the Ethical Committee at Faculty of Dentistry, Ain Shams University, Cairo, Egypt (27-7-2015-Endo). All international and institutional guidelines for animal use and care were followed up.

Animal model

Induction of periapical lesion, root canal obturation, and apical surgery were performed in 36 mandibular premolar teeth (2nd, 3rd, and 4th premolars) in six adult (2–3 years) mongrel male dogs.

Induction of periapical pathosis

After fasting for 12 h, the animals were given subcutaneous atropine sulphate at a dose of 0.05 mg/kg (Atropine sulfate 1%®, ADWIA Co., Egypt) and intramuscular Xylazine HCl at a dose of 1.1 mg/kg (Xylaject® 2%, ADWIA Co., Egypt). Induction of anesthesia was carried out by intravenous Ketamine HCl at a dose of 5 mg/kg (Keiran®, EIMC Pharmacuticals Co., Egypt). To maintain the anesthesia, Thiopental sodium (Thiopental sodium®, EPICO, Egypt) was injected intravenously at adose of 25 mg/kg as incremental doses of 2.5% solution. All teeth were examined radiographically to establish the baseline periapical tissues for further comparison of the periapical area. The inclusion criteria of the selected teeth included a complete root formation and an absence of any dental or periodontal lesions.

Endodontic access cavity was performed in all teeth by size #2 carbide round bur using the high speed hand piece. Sterile stainless steel files sizes #25, 30, 35 (K-Files®, Kerr Company, Scafati, Italy) were used to remove the pulp. A sterile cotton soaked with dogs, plaque suspension was placed in the pulp chamber. The access cavity was left open for a month. Carprofen (Rimadyl tab®, Pfizer Co., USA) was given daily at a dose of 4.4 mg/kg for pain control during the infection time. The teeth were imaged radiographically after 1 month to confirm the periapical pathosis.

Root canal instrumentation and obturation

The dogs were re-anesthetized and the previously infected teeth were re-accessed and the cotton peice was removed. The root canal length was determined using the electronic apex locator (Denjoy iFive Electronic Apex Locator®, Denjoy Dental Company, China) and K file # 15, 20, or 25 according to the initial size of the root canal. Mechanical preparation was accomplished with the Endomotor EndoMate DT (NSK Nakanishi Inc, Tokyo, Japan) using protaper universal rotary files (Dentsply Maillefer, Ballaigues, Switzerland) to master apical file F2, F3, F4, or F5 according to the size of the initial file. Copious irrigation with 20 mL of 5.25% sodium hypochlorite (Chlorox®, Cario, Egypt) and ethylene diamine tetra acetic acid (EDTA) gel 17% (MD Cleanser®, Meta-Biomed Co., Cheongju, Korea) was used during the mechanical preparation. Paper points were used to dry the root canals. These canals were filled by laterally compacted protaper gutta-percha with Adseal resin sealer (Adseal®, Meta-Biomed Co., Cheongju, Korea). The access cavities were sealed by Medifil glass ionomer filling material (Promedica, Toledo, Ohio, United States). One week later, periapical surgeries were performed in both groups.

Surgical procedures

Under the same general anesthesia and aseptic conditions, a full thickness mucoperiosteum flap with two vertical incisions was performed bilaterally in each dog using Bard Parker blade #15 (Aspen Surgical Company, Caledonia, USA). A proper reflection of flaps was done using a suitable sized periosteal elevator. Adequate retraction of the flap was done using Minnesota retractor rested on sound bone to avoid injury of the flapped tissues. The retracted tissues were kept moist with saline solution throughout the surgery. The dimensions of the bony defects were standardized in all dogs. The root apex was approximately localized through the determined canal length, then the periapical buccal bones were excised with a water cooled high speed rotary instrument using a large surgical round bur (minimum size = ISO 016 [US 6]) and a fissure bur (size = ISO 012), creating osseous cavities of 4 mm in diameter and 4 mm in depth.[13] Three millimeters of each root end were resected at a right angle by a fissure cross cut bur. The irregularities of cut surface were removed with a fine flame-shaped diamond bur. Root end resection was performed in all roots included in the defect. The gutta-percha at the resected part of the root was softened using hot instrument to create a good apical seal at the end of the resected root. The operation field was rinsed with sterile saline and the bony defects were packed with epinephrine impregnated gauze to provide hemostasis. After 5 min, the pack in bony crypts was removed and the cut surfaces were wipped with a cotton pellet soaked with sterile saline. Then, the site of surgery was cleaned with sterile saline solution. According to the treatment protocol, the bone defects were classified into two groups; Group I (Control): the bony defects were left empty without placement of any material and Group II (Experimental): the bony defects were filled with synthetic bone graft (G-bone®, Surgiwear Company, India) and covered with PRF. The bone granules (HA granules with average diameter 0.8–1.8 mm) were carried using a bone curette and placed in the bony defects. PRF was prepared as recommended. Briefly, 10 mL of blood were collected from the jugular vein of each dog in a tube without anticoagulant. The tube was immediately centrifuged (Hunan Kaida Scientific Instruments Co., ltd, China) at 3000 rpm for 10 min. A fibrin clot (PRF) was obtained in the middle of the tube, just between the red corpuscles at the bottom and acellular plasma at the top. The PRF clot was separated using tweezers and lancet then placed on the top of each defect as a membrane covering the previously placed bone graft.

The flaps were repositioned in place after placement of the materials and sutured using sterile synthetic absorbable suture #3/0 (Polyglactin 910®, Shanghai Intrag Medical Techs Co., Ltd., Shanghai, China).

Postoperative care included; intra-muscular injections of cefotaxime sodium at a dose of 10 mg/kg (Cefotax 250mg vial®, T3A Co., Egypt) and Diclofenac sodium at a dose of 1.1 mg/kg (Voltaren 75 amp®, Novartis Co., Egypt) once daily for 5 post operative days.[14] The stitches were dressed 3 times daily with povidone-iodine antiseptic solution (Povidone iodine solution®, Amoun Co., Egypt) and removed 10 days post-operative. Each group was further subdivided into two equal subgroups according to the evaluation time, subgroup (A): After 1 month and subgroup (B): after 3 months.

Radiographic evaluation

Radiography of each experimental and control tooth was carried out preoperative, after induction of periapical lesions, immediate post obturation and after 1 month and 3 months of treatment.

Radiographs were taken using a conventional D speed film. A Rinn (XCP) film holder (Dentsply Rinn, USA) was used to ensure standardization of all images. Images were taken using X-ray imaging machine (Fischer, Germany). The conventional films were digitized and image analysis was performed using Digora image analysis software (Digora for windows®, Soredex, Finland) to estimate the periapical bone density quantitatively. The degree of density ranged between zero that corresponded to black and 256 that corresponded to white. To eliminate intra-observer error, the investigation was done by the same radiologist at two different times, with 1 week interval. The values of both trials were pooled, and the mean was calculated. The percentage of difference in periapical radiodensity was calculated between the induction period and after 1 month of treatment and between 1 month and 3 months after treatment.

Histopathologic evaluation

According to the subgroups, an amount of 20 mL of 5% thiopental sodium solution (anesthetic over dose) was rapidly injected intravenously to euthanize the dogs. Mandibles of each dog were resected and blocks containing each tooth with its surrounding bone were fixed in 10% formalin solution for 7 days. The specimens were decalcified using 17% EDTA solution that refreshed every 48 h for 90 days. The samples were processed by the conventional method. Breifly, the specimens were dehydrated by increasing concentrations of alcohol (50%, 60%, 80%, 90%, and absolute alcohol), then cleared in xylene and embedded in paraffin blocks. 5 μm serial sections of each specimen were made for the subsequent hematoxylin and eosin staining. The specimens were examined under a light microscope (BX60, Olympus, Japan) for inflammatory cell count, measurement of bone area fraction, and qualitative evaluation as follows.

Inflammatory cell count

From each section, 3 microscopic fields of the periapical region were captured at original magnification of ×40 for the inflammatory cell count. The inflammatory cells were counted after determining the range of inflammatory cell size from 457 to 4450 pixels and circularity from 0.3 to 1 [Figure 1].
Figure 1: The steps of inflammatory cell count: (a) The original image. (b) The original image after conversion to gray scale. (c) The image threshold and color coding for selection of the most of the cells in the picture. (d) The software automatically generated a thresholded black and white binary image. (e) Inflammatory cell count after exclusion of the undesired cells (on the basis of size and circularity)

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All images were captured by a digital camera (C5060, Olympus, Japan) that was connected to the light microscope. After transferring the images to the computer, inflammatory cell count was carried out using image analysis software (Image J, 1.41a®, NIH, USA).

Measurement of the bone area fraction

Two fields at original magnification ×20 were obtained for each section. The newly formed bone was detected in the area beneath the apicectomy then, the image was converted to 8-bit type. A threshold was adjusted to the newly formed bone and the area fraction of new bone was measured. The mean of the two fields was obtained for each section. To eliminate the intra-examiner variability, the examination was repeated by the same pathologist after 1 week. The values of both examinations were pooled, and the mean was calculated [Figure 2].
Figure 2: Steps of the measurement of bone area fraction: (a) Original image. (b) Eight-bit image. (c) Threshold image. (d) Analyzed image

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Qualitative evaluation

A complete description of the characteristics of the periapical region of each group was done at magnifications ×200–400.

Statistical analysis

All data were entered into the Statistical Package for Social Science (IBM SPSS version 23, USA). Kolmogorov–Smirnov and Shapiro–Wilk tests were applied to examine the normality of data. The quantitative data were presented as mean, standard deviations, and ranges while qualitative variables were presented as number and percentages. To compare the qualitative data of both groups, Chi-square test and/or Fisher's exact test were applied when the expected number in any cell found <5. To compare the quantitative data of both groups, Paired t-test and Wilcoxon Rank test were performed with parametric distribution and nonparametric data, respectively. The confidence interval was adjusted at 95% and the margin of error accepted was adjusted at 5%. The P value was considered significant as follows: P >0.05: Non significant, P < 0.05: Significant(S) and P < 0.01: Highly significant (HS).

  Results Top

Radiographic findings

Radiodensity of the periapical bone

No significant difference was seen in the mean radiodensity between both groups at the end of infection period (induction period) (P > 0.05). While there were HS differences in the mean radiodensity between Group I and II in both A and B subgroups as shown in [Table 1].
Table 1: The mean and standard deviation values of radiodensities of periapical bone in both groups at different time periods

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Group I exhibited a significant difference in the mean radiodensity between the induction period and 1 month period (subgroup A) as well as between the induction period and 3 months' period (subgroup B) (P < 0.05). However, there was no significant difference in the mean radiodensity between subgroup A and subgroup B (P > 0.05).

Group II exhibited a significant difference in the mean radiodensity between the induction period, 1 month period and 3 months' period (P < 0.05) [Figure 3].
Figure 3: Representative radiophotographs of Group II (apicectomy + platelet-rich fibrin + synthetic bone graft) showing measurement of bone density using Digora software after 1 month period (a) and 3 months (b)

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Percentage of difference in radiodensity

There was a HS difference in percentage of difference in radiodensity between both the groups (P < 0.001) from the induction period to 1 month and from 1 month to 3 months.

Group I exhibited no significant difference in the percentage of difference in radiodensity from the induction to 1 month after treatment (7.95 ± 4.70) and from 1 month to 3 months after treatment (3.12 ± 7.69) (P > 0.05). While in Group II, there was a HS difference in the percentage of difference in radiodensity from the induction to 1 month (28.69 ± 10.26) and from 1 month to 3 months (44.95 ± 13.01) (P < 0.001).

Histopathological findings

There were HS differences between Group I and II in the mean inflammatory cell count and the percentage of newly formed bone (P < 0.001). No significant difference was recorded between both subgroups in Group I and II (P > 0.05) regarding the mean inflammatory cell count. In contrast to Group I, there was a HS difference in the percentage of newly formed bone between both subgroups in Group II (P < 0.001).

Results of the inflammatory cell count

In Group I, the mean inflammatory cell count was 211.53 ± 101.39 and ranged between 34 and 381 after 1 month while it was 153.13 ± 95.15 and ranged between 26 and 310 after 3 months.

In Group II, the mean inflammatory cell count was 61.20 ± 25.71 and ranged between 4 and 190 after 1 month while it was 20.20 ± 10.12 and ranged between 8 and 38 after 3 months.

Results of measurement of the bone area fraction

In Group I, after 1 month (subgroup A), the percentage of newly formed bone ranged between 0 and 16.36 (Mean: 9.41 ± 5.05) while it ranged between 4.3 and 22.5 (Mean: 12.47 ± 6.61) after 3 months (subgroup B).

In Group II, the mean of percentage of newly formed bone was 23.93 ± 11.48 and ranged between 5.3 and 41.51 after 1 month of treatment while it was 53.58 ± 10.16 and ranged between 38.5 and 70.25 after 3 months.

Qualitative findings

Group I, after 1 month showed inflammatory cell infiltrates, some collagen bundles interlaced with the inflammatory cells, cells resembling the fibroblasts [Figure 4]a and small bony spicules toward the periphery [Figure 4]b. After 3 months, a network of collagen fibers was seen with very few bundles of inflammatory cells in the central zone [Figure 4]c. Bone trabeculae were more abundant and interlaced with collagen fibers and fibroblastic cells. No inflammatory infiltrate was demonstrated in any of these samples [Figure 4]d.
Figure 4: (a) Representative photomicrograph for Group I after 1 month of apicectomy showing low-grade inflammatory cell infiltrates, collagen bundles (black arrow) interlacing with inflammatory cells, and fibroblasts resembling cells (H and E, ×400). (b) Notice the small bony spicules (black arrow) toward the periphery (H and E, ×200). (c) Group I after 3 months of apicectomy showing a network of collagen fibres with very few bundles of inflammatory cells (black arrow) (H and E, ×400). (d) Group I after 3 months of apicectomy showing bone trabeculae (black arrow) interlaced with collagen fibres, fibroblastic cells, and no inflammatory infiltrates (H and E, ×200)

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Group II after 1 month exhibited inflammatory infiltrates with highly populated chronic inflammatory cells. Networks of collagen fibers were seen at the periphery with numerous fibroblasts [Figure 5]a. Osteoid matrix with osteoblastic rimming was also detected [Figure 5]b. After 3 months, heavy strands of connective tissue fibers were seen with numerous fibroblasts. These connective tissue fibers were separated in some areas with few inflammatory cells [Figure 5]c. Moreover, the peripheral alveolar bone exhibited remodeling with new bone formation [Figure 5]d.
Figure 5: (a) Photomicrograph for Group II after 1 month of apicectomy showing inflammatory infiltrates, highly populated chronic inflammatory cells (blue arrow), networks of collagen fibers and fibroblasts (black arrow) (H and E, ×400). (b) Photomicrograph for Group II after 1 month of apicectomy showing osteoid matrix with osteoblastic rimming (H and E, ×200). (c) Group II after 3 months of apicectomy showing heavy strands of connective tissue fibres, fibroblasts, and inflammatory cells (H and E, ×400). (d) Group II after 3 months of apicectomy showing remodeling of peripheral alveolar bone and new bone formation (black arrow) (H and E, ×200)

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  Discussion Top

The presence of apical periodontitis significantly affects the success of endodontic treatment.[15] These teeth usually managed by either nonsurgical retreatment or periapical surgery.[16] Endodontic surgery is usually done when the primary as well as secondary endodontic therapy is failed.

The choice of PRF in this study was based on its excellent handling characteristics, easily preparation and manipulation, well tolerance, and enhancement of healing of both soft and hard tissues.[17],[18] The synthetic bone graft used in this study is considered among the first bone substitutes. The HA content of the synthetic bone graft binds to bone and accelerates the bone healing through the activation of osteoblasts.[19]

In order to simulate the clinical conditions, the dogs, teeth were left open for a month to induce periapical pathosis.[20],[21]

Image analysis was done using Digora software (Digora for windows, Soredex, Finland) that calculates the radiographic density (bone mineral density) by means of its gray levels. Digora determines the differences between analyzed areas in pixels, to obtain numeric data about bone density alterations.[22] In this regards, Delano et al. found that digital subtraction method may be useful assessment in endodontic apical surgery due to the significant radiometric correlation with histology.[23]

Group II had higher value of percentage of difference in radiodensity of periapical bone than Group I due to the presence of PRF in Group II which is a fibrin network rich in blood platelets, cytokines, growth factors, and leukocytes.[24] In addition, PRF is an autogenous gelatinous material that enhances the clot and graft stability, regulates inflammation, stimulates the chemotaxis of stem cells and accelerates healing. Moreover, the HA used in Group II is a biocompatible ceramic material that has the ability to bind to bone without inducing inflammatory or toxic reactions and shows osteoconductive properties.[25]

In addition, Group II exhibited a significant difference in percentage of difference of periapical radiodensity between both subgroups; here the time was an important factor in increasing the difference in the percentage of radiodensity due to the presence of PRF which accelerates bone regeneration through attracting the stem cells by time. This is in agreement with the results of earlier workers.[1] On the other hand, Garret et al. found that placement of a guided tissue membrane over the induced bony defect during the endodontic peri-apical surgery for 3, 6, and 12 months has no beneficial effect on the rate of healing and adds expense on the patient.[26]

Moreover, the osseointegration of HA bone graft allows the reconstruction of the bone defects without the need of allogeneic or autogenous bone grafts,[27] especially when nano crystalline HA is used in combination with PRF.[18] In contrast, Caplain et al. used demineralized bone matrix covered with expanded poly tetra fluroethelyne (PTFE) membranes in induced dog's jaw defect for 4 weeks without any positive histological effects of PTFE on bone healing.[28] This controversy may be due to the differences in the type of bone graft and membrane used in this study (synthetic HA bone + PRF). Moreover, the evaluation period in Caplin's study was 4 weeks which is not enough in comparison to the present study that extended to 3 months. In addition, Bernabe et al. found that the application of membrane and bone graft either alone or together with apical surgery did not change the periapical healing following root end filling with mineral trioxide aggregate (MTA).[29] This controversy may be due the difference in bone graft and membrane used and using of MTA which is a retrofilling material of excellent properties leading to favorable tissue healing.[30] However, Britain et al. recorded that adding of bone graft to the membrane provides no benefits compared with the application of the membrane alone. This may be due to the size of bony defects, the differences in types of bone graft and membranes used and the evaluation periods.[31]

The addition of GTR to the endodontic surgery usually promotes the bone healing and improves the outcome in large periapical lesions.[1] Therefore, this work investigated the efficacy of PRF in conjunction with synthetic bone graft on the healing of the periapical bone defects after apicectomy. The study concluded that adding of PRF and synthetic bone graft after apicectomy has a favorable outcome than apicectomy alone.

The main limitations of this study were the limited sample size and the short evaluation times. Further studies are recommended to investigate the healing potential of this regeneration technique in larger periapical bony defects than that used in the current study and to apply the regenerative technique or materials used in this study on humans.

  Conclusions Top

Using of PRF in conjuction with the synthetic bone graft enhances the healing of periapical intrabony defects after apicectomy in dogss' teeth.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]

  [Table 1]


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