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Research Article

Platelet-rich Fibrin Membrane Combined with Beta-Tricalcium Phosphate for Treatment of Infrabony Defects in Chronic Periodontitis: A Case Series

Kazuhiro Okuda*1, Yu Nakajima1, Tomoyuki Kawase2, Mito Kobayashi1, Mana Kamiya1, Makoto Horimizu1, Larry F. Wolff 3, Hiromasa Yoshie1

1Division of Periodontology, Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences,
2Division of Dental Pharmacology, Department of Tissue Regeneration and Reconstruction, Niigata University Graduate School of Medical and Dental Sciences, 2-5274 Gakko-cho, Chuo-ku, Niigata 951-8514, Japan
3Division of Periodontology, Department of Developmental and Surgical Sciences, University of Minnesota School of Dentistry, 17- 164 Moos Health Science Tower, 515 Delaware Street S.E., Minneapolis, MN 55455, USA

*Corresponding author: Dr. Kazuhiro Okuda, Division of Periodontology, Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences, 2-5274 Gakko-cho, Chuo-ku, Niigata 951-8514, Japan, Tel: +81 25 227 2870; Fax: +81 25 227 0808; E-mail: okuda@dent.niigata-u.ac.jp

Submitted: 06-26-2015  Accepted: 07-23-2015 Published: 08-10-2015

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Article

 
Abstract

This open cross-sectional questionnaire study investigated subjective oral symptoms in hospitalized psychiatric patients, comparing those taking typical vs. atypical neuroleptic drugs. The present study included 170 hospitalized patients who were taking psychiatric medications. We observed a significantly higher prevalence of xerostomia in the typical neuroleptic group (66%) compared with the atypical neuroleptic group (53%, p<0.01). In our study, 28% of women and 17% of men received professional consultations for dry mouth. Persistent oral pain lasting throughout the day was reported by 46% and 5% of patients in the typical and atypical neuroleptic groups, respectively. The oral pain was predominantly located in the tongue and buccal mucosa; it was described as a burning sensation by patients in both medication groups. These results emphasize the need for awareness of oral discomfort and its subsequent effects on quality of life in this challenging patient group.

Keywords: Platelet-rich Fibrin; Beta-Tricalcium Phosphate; Angiogenic Growth Factors; New blood vessels; Periodontal regeneration; Regenerative Medicine


Introduction

Advances in tissue engineered techniques using the three key elements; scaffolds, growth and differentiation factors, and cells have provided opportunities for a new regenerative treatment of periodontal defects [1-5]. In addition, it has been demonstrated that angiogenesis is also one of the most important factors in repair or regeneration procedures [6,7]. Growth and differentiation factors such as PDGF, IGF and TGF-β regulate key events in wound healing, including chemotaxis, differentiation, proliferation, and matrix synthesis. In previous studies, it has been demonstrated platelet-rich plasma (PRP) contained PDGF and TGF-β isoforms at greater levels, and significantly stimulated cell proliferation and neo-vascularization [8-10]. In an earlier reported clinical study, a combination of PRP combined with hydroxyapatite(HA) granule bone grafts in the treatment of infrabony periodontal defects offered a significantly more favorable clinical improvement in probing depth reduction, clinical attachment gain and vertical relative attachment gain 12 months after surgery [11]. However, the protocol of PRP preparation is relatively complicated; operators need to be trained to collect the maximum amount of the buffy coat without collecting red blood cells. In addition, although being less technique-sensitive, the centrifugation process needs to be optimized. Otherwise, platelets would be over-activated allowing the release and loss of vital growth factors more than warranted to achieve optimal repair or regeneration. Moreover, in the absence of added anti-coagulants, it is possible that activation of the endogenous coagulation system could lead to activation of platelets and subsequent loss of growth factors.

Recently, Platelet-rich fibrin (PRF) was introduced by Choukroun and his co-workers [12,13]. This group of investigators developed a novel technique to clot liquid PRP solely by stimulating the endogenous coagulation pathway. PRF preparations, when compared to PRP preparations, are less influenced by operator skills. This so-called “second generation of PRP” is designated PRF and has been increasingly substituted for PRP in regenerative medicine. In a recently published in vitro study reported by Kobayashi and co-workers, PRF preserved bioactive growth factors such as PDGF-BB, EGF, FGF-4, IGF-II, PDGF-AB and VEGF-D, and stimulated an increase in the number of new blood vessels [14].

A number of inorganic synthetic graft materials are available for use in the treatment of periodontal infrabony defects. Histological evidence indicated that synthetic grafts act almost exclusively as biological fillers, with scant bone fill and very limited connective tissue regeneration [15, 16]. β-TCP is included in the synthetic absorbable graft materials, has biocompatibility and based on histological studies has demonstrated osteoconductivity [17-19]. On the other hand, β-TCP has not been shown to have the potential for initiating, enhancing or stimulating new attachment apparatus and new blood vessel formation. Therefore, the use of PRF in combination with the osteoconductive, synthetic scaffold β-TCP granules for periodontal regeneration therapy offers an interesting and potentially clinically useful modality to the clinician in treating periodontal osseous defects in humans. Therefore, the purpose of this investigation is to present thirteen cases from a twelve month clinical trial addressing this novel approach of regenerating infrabony osseous defects in humans.

Material and Methods

Patients with advanced chronic periodontitis were recruited and scheduled to receive periodontal therapy at Niigata University Medical and Dental Hospital. The study design and consent form were approved by the ethical committee for human subject use at Niigata University Medical and Dental Hospital in accordance with the Helsinki Declaration of 1975 as revised in 2013. The criteria for inclusion of patients and periodontal sites in the study were 1) non-smoking, free of systemic complications and no history of allergies, 2) no use of antibiotics over the previous 6 months prior to treatment, 3) no treatment for periodontitis during the previous 2 years, 4) presence of one infrabony defect with a probing depth (PD) ≥6 mm, clinical attachment level (CAL) ≥6 mm, osseous defect depth estimated to be ≥3 mm as measured radiographically and 5) presence of at least 2 mm of keratinized gingiva on the facial aspect of the selected tooth.

Prior to the surgical procedures, initial periodontal therapy was performed on all patients. Presurgical treatment consisted of stringent plaque control repeated until patients achieved a Modified O’Leary plaque score [20] of 10 % or less, full-mouth scaling and root planing under local anesthesia, and occlusal adjustment if trauma from occlusion was present. After completion of the initial therapy, a re-evaluation examination was performed 3 months later to determine patient response to the treatment provided and to confirm the need for periodontal surgery. Fifteen patients were initially enrolled in this study.

Clinical measurements included probing depth (PD), measured as the distance from the free gingival margin to the probeable base of the pocket, clinical attachment level (CAL), measured from the cemento-enamel junction (CEJ) to the base of the pocket by using a calibrated color-coded periodontal probe to the nearest mm (HuFriedy Mfg., Inc, Chicago, IL, USA) and customized acrylic stents with a guiding groove. For radiographic measurements, a commercially available film holder device (Hanshin Technical Laboratory, Ltd., Hyogo, Japan) was modified by placing registration material on the bite block to index the dentition. Standardized radiographs using a paralleling cone technique with positioning aids, were taken at baseline, 3, 6 and 12-month post-surgical evaluation time periods. Radiographic infrabony defect depth (IBD) was assessed using the method described by Cardaropoli and Leonhardt in 2002 [21]. Briefly, the IBD was measured as the radiographic vertical dimension between the projection of the osseous crest adjacent to the root surface (BCP) and the most coronal osseous level adjacent to the root surface where the periodontal ligament space was considered to have a normal width (BoBD). The infrabony osseous defect was then measured by the following calculation: IBD=BCP-BoBD. The twelve-month healing result of each treated osseous defect site was assessed and the difference between baseline and twelve months for the clinical values (PD and CAL) and radiographic values (IBD) were determined.

The PRF membrane preparation procedure was described in a previous report [14]. Briefly, blood was collected from each patient using butterfly needles (21G × 3/4’’; NIPRO, Osaka, Japan) and VacutainerTM tubes (Japan Becton, Dickinson and Company, Tokyo, Japan). To prepare the PRF, the collected blood samples were immediately centrifuged by a Medifuge centrifugation system (Silfradent S. r. l., Santa Sofia, Italy). Preparation of the PRF membrane is shown in Figure 1. After eliminating the red thrombus, the resulting PRF preparation (Figure 1(a)) was compressed by the PRF compression device (Figure 1(b)). The stainless steel PRF compression device developed for PRF membrane preparation is composed of two spoon shaped parts. The clearance of both spoon parts was adjusted to be 1 mm. Thus, when the PRF clot was compressed with this device, a standard 1-mm thick PRF membrane was consistently prepared.

Figure 1. Preparation of the PRF membrane.

a) Platelet-rich fibrin created just after centrifugation

 
dentistry  fig 22.1a
 
b) PRF membrane compression device
 
dentistry  fig 22.1b
 
Periodontal surgical procedures were performed on an outpatient  basis under aseptic conditions by two trained periodontal clinicians (authors KO and YN). After providing local anesthesia to patients, crevicular incisions were made and full-thickness mucoperiosteal flaps were elevated. Vertical releasing incisions were performed only if necessary for betteraccess or to achieve more favorable closure of the surgical site. The surgical procedure fully exposed the infrabony defects and preserved the marginal gingiva and interdental tissue. Meticulous defect debridement and root planing were carried out to remove visible subgingival plaque, calculus, inflammatory granulation tissue and pocket epithelium. The surgical sites were thoroughly rinsed with sterile saline and care was taken to keep the area free of saliva and blood. The β-TCP granule graft material (Cerasorb® M; curasan AG, Kleinostheim, Germany) was then reconstituted in sterile saline and placed into the defects using amalgam condensers to the vertical height of the corresponding adjacent bone level of the infrabony defect. Then, PRF membranes were overlaid onto the β-TCP granule. The surgical flaps were repositioned to their presurgical levels and sutured with 5-0 nylon suture utilizing an interrupted, vertical mattress technique. Postoperative care included systemic administration of cefcapene pivoxil hydrochloride (FLOMOX ®; Shionogi & Co., Ltd., Osaka, Japan) at 300 mg per day for five days and a 5% povidone iodine (ISODIN®; Meiji Seika Pharma Co., Ltd., Tokyo, Japan) rinse three times daily for six weeks. Sutures were removed at two weeks postsurgery. After suture removal, patient plaque control using the roll tooth brushing technique utilizing an ultra soft toothbrush was resumed at the surgically treated sites. Supragingival professional tooth cleaning was also performed weekly for the first six weeks postsurgery and thereafter the patients were recalled once a month up to twelve months post-surgery for oral hygiene reinforcement and prophylaxis.

Statistical analysis

Taking into account the paired nature of the changes from baseline to 12 months, the Wilcoxon signed-rank matched pair test was performed for the pairwise statistical analysis of these data. The null hypothesis was rejected when the risk percentage was below 5% (p <0.05).

Results

Of the 15 patients initially enrolled in thie clinical trial, 13 (7 men and 6 women) completed the study (13 sites). The two patients who were dropped from the data analysis did not return for all their follow-up appointments. Age range of subjects was 40 to 65 years with a mean age of 48.1 ± 6.3 years. There were no patient reported infectious episodes and no other adverse complications associated with treatment over the 12 month time period of this study.

Clinical and radiographic results from 13 patients at baseline and after 3, 6 and 12 months following treatment of infrabony defects with the PRF membrane and β-TCP phosphate are shown in Table 1. Patient compliance with the supportive periodontal therapy was excellent, and the 13 patients included in the data analysis visited the clinic monthly and received maintenance care which included oral hygiene instruction, mechanical tooth polishing and scaling. Patient’s oral hygiene level and infection control were maintained at a high level throughout the study period. Accordingly, the full-mouth plaque score (FMPS) and full-mouth bleeding score (FMBS) remained <10% throughout the entire study, and no significant differences were seen between the evaluation points (data not shown). Individual infrabony defect location and morphology is summarized as follows; Seven defects were located in the maxilla and six were in the mandible. Of the 13 infrabony defects, 3 were two-wall defects and 10 were three-wall defects. The 12-month results after treatment demonstrated the mean PD, CAL and IBD values were improved significantly when compared to baseline (PD: 3.1 ± 0.3 mm at 12-months versus 7.9 ± 1.6 mm at baseline, p <0.01; CAL: 6.6 ± 1.3 mm at 12-months versus 9.5 ± 1.9 mm at baseline, p <0.01; IBD: 1.9 ± 1.0 mm at12-months versus 5.1 ± 1.9 mm at baseline, p <0.01).

dentistry  table 22.1

 
* PD = Probing Depth, CAL = Clinical Attachment Level, IBD = Radiographic Infrabony Defect Depth.

† Statistical significance level between baseline and 12 months in the treatment group. Statistical significant, p <0.01.

Table 1. P robing depth, clinical attachment level and radiographic infrabony defect depth (mean ± SD) at baseline and after three, six and twelve months following treatment of infrabony defects with the PRF membrane and beta-tricalcium phosphate.

 
Case reports

Radiographic and clinical observations including treatment of an infrabony osseous defect is shown in Figures 2 and 3.

Case 1

A 49-year-old Japanese male, presented with radiographic evidence of bone loss on the mesial surface of the maxillary left canine (Figure 2(a)). The clinical measures of PD and CAL of 9 and 12 mm, respectively, were observed at baseline (Figure 2(b)). At the time of periodontal surgery, a 5-mm-incisal-apical by 5 -mm- mesio-distal osseous defect was observed. A threewalled infrabony osseous defect on the mesio-labial surface of the canine was revealed (Figure 2(c)). After debridement, β-TCP granules were placed into the osseous defect and overlaid with the PRF membrane (Figure 2(d, e)), and then sutured (Figure 2(f)). At 12 months postsurgery, PD and CAL measurements were 3 and 6 mm, respectively (Figure 2(g)). Increased radiopacity was apparent on the treated mesial surface of the canine (Figure 2(h)).

Figure 2 (Case 1). Radiographic and clinical onservations along with treatment of an infrabony osseous defect using the PRF membrane and β-TCP.

dentistry  fig 22.2a

a) Baseline periapical radiograph showing bone loss on the mesial surface of the maxillary right canine ( arrow-head ).

dentistry  fig 22.2b

b) Baseline clinical appearance on the mesial surface of the maxillary left canine.

dentistry  fig 22.2c
 
c) Intraoperative facial view of the 3-walled infrabony defect.
l dentistry  fig 22.2d
 
d) Intraoperative facial view of surgical site following placement of β-TCP granules.
  dentistry  fig 22.2e
e) Intraoperative facial view of surgical site following placement of the PRF membrane covering β-TCP granules.
 
dentistry  fig 22.2f
f) Intraoperative facial view of surgical site following suturing
dentistry  fig 22.2g 
g) Clinical measurements at 12 months post-surgery.
dentistry  fig 22.2h
h) Radiopaque fill of the mesial osseous defect at 12 months post-surgery( arrow-head ).
 
Case 2

A 47-year-old Japanese male, presented with radiographic evidence of bone loss on the distal surface of the maxillary right first molar (Figure 3(a)). The clinical measures of PD and CAL of 9 and 9 mm, respectively, were observed at baseline (Figure 3(b)). At the time of periodontal surgery, a 6-mm-incisal-apical by 3 -mm- mesio-distal osseous defect was observed. A two-walled infrabony osseous defect on the distal surface of the first molar was revealed (Figure 3(c)). After debridement, a β-TCP granule graft was placed into the osseous defect and overlaid with the PRF membrane (Figure 3(d, e)), and then sutured (Figure 3(f)). At 12 months postsurgery, PD and CAL measurements were 3 and 6 mm, respectively (Figure 3(g)). Increased radiopacity was apparent on the treated distal surface of the first molar (Figure 3(h)).

Figure 3 (Case 2). Radiographic and clinical observations along with  treatment of an infrabony osseous defect using the PRF membrane and β-TCP.

 
dentistry  fig 22.3a
 
a) Baseline periapical radiograph showing bone loss on the distal surface of the maxillary right first molar (arrow-head ). Arrow marks base of original defect.


dentistry  fig 22.3b

b) Baseline clinical appearance on the distal surface of the maxillary
right first molar.

dentistry  fig 22.3c

c) Intraoperative facial view of the 2-walled infrabony defect.

dentistry  fig 22.3d

d) Intraoperative facial view of surgical site following placement of β-TCP granules.
 dentistry  fig 22.3e
 
 e) Intraoperative facial view of surgical site following placement of the PRF membrane covering β-TCP granules.

dentistry  fig 22.3f

 
f) Intraoperative facial view of surgical site following suturing.
dentistry  fig 22.3g
 
g) Clinical measurements at 12 months post-surgery.

dentistry  fig 22.3h

 
h) Radiopaque fill of the distal osseous defect at 12 months post-surgery (arrow-head ). Arrow marks base of original defect.
 
Discussion

The PRF membrane in combination with an osteoconductive, synthetic scaffold of β-TCP granules were successfully used in the treatment of thirteen human infrabony defects to achieve favorable clinical results. The clinical results from these cases demonstrated this novel regenerating approach was effective in improving clinical and radiographic parameters between baseline and 12 months.

The PRF membrane together with the β-TCP granule treatment showed an average PD reduction of 4.8 mm, a CAL gain of 3.9 mm, and the radiographic infrabony defect depth difference of 3.2 mm at 12 months post-surgery. A previous reported clinical trial from our research group evaluating treatment of infrabony defects with PRP + HA found a PD reduction of 4.7 ± 1.6 mm, a CAL gain of 3.4 ± 1.7 mm and a radiographic defect change of 3.5 ± 1.5 mm at 12 months post-surgery [10]. The clinical results with PRF membrane +β-TCP granules were clinically similar to just PRP + HA granule treatment. Chang et al., reported that PRF application exhibited pocket reduction and gain in clinical attachment along with increased post-operative radiographic bone density in the treated defects [22]. Pradeep and Sharma also found greater reduction in probing depth, greater gain in periodontal attachment level and greater bone fill in 3-wall intrabony defects treated with PRF and open flap debridement (ODF) when compared to ODF alone [23].


The factors very likely contributing to these more favorable clinical results would be the significant increase in the number of matured blood vessels as well as angiogenic growth factors such as PDGF and VEGF which would provide greater regeneration potential of the graft. In a previous in vitro and animal study evaluating PRF using an ELISA assay, cell culture and scratch assay, western blotting analysis, the chorioallantoic membarane (CAM) assay and histological and immunohistochemical examination, it was found that 1) angiogenic growth factors such as PDGF and VEGF were concentrated when compared with platelet-poor plasma, 2) PRF preparations had an enhanced effect on phosphorylation of VEGFR2 in human umbilical vein endothelial cells (HUVECs) and 3) PRF preparations favorably improved new blood capillary formation, and 4) also favorably impacted the thickness and structure of the CAM and the formation of mature blood vessels in the CAM [14].

Another factor that should be considered in interpreting our favorable clinical results in treating human osseous defects is the network of fibrin fibers which is one of the major structural components in PRF. Previously it has been observed by SEM examination that platelets aggregated and attached on the fibrin surface of PRF membranes [14, 25], and therefore, the PRF membrane may function to serve as a storage of growth factors before their release from platelets. In addition, the PRF membrane with its fibrin network may act like a bandage that accelerates the healing of wound edges. The PRF membrane may also provide significant postoperative protection of the surgical site and may hasten the integration and remodeling of the grafted biomaterial [24, 25]. Among the factors likely contributed by the PRF membrane to the favorable clinical results would be the positive clinical effect of β-TCP granules serving as a scaffold to maintain space making and the osteoconductivity nature of the β-TCP grafting material [22-24].

Conclusion

Within the clinical trial design limits of this case series, PRF membranes in combination with β-TCP granules demonstrated a favorable clinical improvement in treating infrabony osseous defects. In the future, clinical studies involving a greater number of human subjects in a randomized controlled clinical trial study design and monitoring for a longer period of time would be necessary to definitively prove the clinically favorable results we reported here for this new tissue engineered grafting procedure in treating periodontal osseous defects.

 
Declaration of interests:

The authors have no commercial, proprietary, or financial interest in the products or companies described in this article.


Acknowledgments

This study was supported by the Japanese Society for the Promotion of Science (KAKENHI; Grant No.24390465
 
 

References

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Cite this article: Okuda.Platelet-rich Fibrin Membrane Combined with Beta-Tricalcium Phosphate for Treatment of Infrabony Defects in Chronic Periodontitis: A Case Series. J J Dent Res. 2015, 2(3): 022.

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