This case report aimed to describe the effects of leukocyte and platelet-rich fibrin (L-PRF) associated with demineralized bovine bone mineral (DBBM) and absorbable collagen membrane (CM) on bone regeneration in maxillary sinus augmentation. A 59-year-old male patient was referred to the Department of Periodontology for implant rehabilitation of his edentulous upper jaw. The treatment plan involved maxillary sinus augmentation followed by implant installations. A split-mouth design was employed in which the right maxillary sinus was filled using L-PRF, DBBM, and CM; the left side was filled with DBBM and CM. After 4 and 8 months postoperatively, 2 dental implants were installed in each of the right and left maxillary sinuses. Cone-beam computerized tomography (CBCT) was taken before and after sinus augmentation for evaluation of tridimensional bone volume alterations. Bone biopsies were harvested from the implant sites for histomorphometric evaluation. Resonance frequency analysis was employed immediately after implant placement and before prosthetic rehabilitation for evaluation of implant stability. Implants were loaded 10 months after sinus augmentation. CBCT analysis showed a higher resorption rate in the right side of the maxillary sinus (L-PRF + DBBM) compared to the left side (22.25% and 8.95%, respectively). Implant stability quotients were above 68 in all time-points for both groups. Histomorphometric analysis showed a high amount of newly formed bone when L-PRF was used compared with DBBM alone (2 118 102 and 975 535 mm3, respectively). Taken together, both techniques were effective for maxillary sinus augmentation, however the addition of L-PRF to the graft allowed early implant placement and accelerated bone healing in the conditions studied.

Introduction

Sinus lift, a surgical approach that enables the placement of appropriate length implants,1  is achieved by means of the elevation of the sinus membrane allowing the interposition of bone grafts for long-term implant stability. Deproteinized bovine bone mineral (DBBM; Bio-Oss, Geistlich Pharma AB, Wolhusen, Switzerland) is an osteoconductive material, chemically and physically similar to human bone; it acts as a scaffold, allowing osteogenic cell transportation from the sinus wall to the graft particles increasing the potential of new bone formation.2,3  To enhance bone formation and accelerate bone healing, we have proposed the addition of leukocyte and platelet-rich fibrin (L-PRF).2,49  Platelets present beneficial effects on tissue healing through release of growth factors, such as platelet-derived growth factor, vascular endothelial growth factor, insulin-like growth factor, and transforming growth factor.5  The unique fibrin form can also promote angiogenesis and osteogenesis,5  which might improve the regeneration of sinus cavities.8  PRF can also modulate the expression of osteoprotegerin, increasing osteoblast differentiation.10  Furthermore, previous studies have demonstrated that L-PRF can be considered an alternative material for repairing sinus perforations11  and for socket management.12  A recent systematic review13  showed promising results when L-PRF was used as the sole filling material, combined with bone substitutes into the maxillary sinus. Additionally, we witnessed accelerated maturation of demineralized dried bone.13  Because of these characteristics, L-PRF has been accepted by the profession and is routinely used in the clinic.14 

Although Bio-Oss, the most utilized DBBM biomaterial, has often been used as a bone substitute,15,16  a small number of studies have addressed the effect of adding L-PRF for maxillary sinus augmentation in combination with DBBM.2,17,18  Moreover, there appear to be no studies that have utilized cone-beam computerized tomography (CBCT) and resonance frequency analysis (RFA) to measure bone volume alterations and implant stability after sinus augmentation with L-PRF. Thus, the aim of this current paper was to report the effects of L-PRF associated with DBBM and collagen membrane (CM) on bone regeneration in maxillary sinus augmentation, as well as the capability of L-PRF in accelerates bone healing for early implant placement.

Case Presentation

A 59-year-old male patient was referred to the Department of Periodontology for implant rehabilitation of his edentulous upper jaw (Figure 1a). He had no relevant medical history that could compromise bone healing19,20  and denied smoking and the use of alcohol. A CBCT scan (iCat Classic, Imaging Sciences International, Hatfield, Pa) was rendered to evaluate the reminiscent vertical bone height (Figure 1b). Given the limited amount of bone height in the posterior area of the maxilla, the proposed treatment plan involved maxillary sinus augmentation followed by implant installation. A split-mouth design was planned in which the right maxillary sinus floor was augmented using L-PRF associated with DBBM (Geistlich Pharma AG) and absorbable CM (Bio-Guide, Geistlich Pharma AG), followed by implant placement after 4 months postsurgery. The left side (control side) was filled with DBBM and CM, and dental implants were installed after 8 months post-sinus augmentation. The patient was informed about the treatment and its possible side effects. The recommended treatment plan was accepted by the patient, and a written informed consent was signed. The study protocol was approved by the Institutional Ethics Committee on Human Research (protocol number 41357514.5.0000.5416).

Figures 1 and 2.

Figure 1. Pre-operative clinical examination. (a) Occlusal. (b) Cone-beam computerized tomography showing the reminiscent alveolar bone and the sinus anatomy. Figure 2. (a) Leukocyte and platelet-rich fibrin (L-PRF) clots in the form of a membrane. (b) Mixture of L-PRF and demineralized bovine bone mineral (Bio-Oss) of 0.25–1 mm particle size.

Figures 1 and 2.

Figure 1. Pre-operative clinical examination. (a) Occlusal. (b) Cone-beam computerized tomography showing the reminiscent alveolar bone and the sinus anatomy. Figure 2. (a) Leukocyte and platelet-rich fibrin (L-PRF) clots in the form of a membrane. (b) Mixture of L-PRF and demineralized bovine bone mineral (Bio-Oss) of 0.25–1 mm particle size.

Case Management

The addition of L-PRF to the bone graft in the right maxillary sinus was used to investigate the capability of this growth factor in accelerate bone healing for early implant placement and to compare it with the well-established protocol using only DBBM in the left sinus. Prior to the maxillary sinus augmentation procedure, L-PRF was prepared according to previous protocols.6,8,21,22  Briefly, a peripheral blood sample was taken before the surgery and immediately centrifuged at 3000 rpm for 10 min using an appropriate centrifuge (Kasvi K14-0815, Kasvi, Curitiba, Brazil). After centrifugation, the fibrin clot was removed from the tube and separated. The L-PRF clot was prepared in the form of a membrane by pressing out the fluids (Figure 2a).23  Subsequently, the L-PRF was mixed with the DBBM (0.25–1 mm particle sizes) to fill the right sinus (Figure 2b) in 1:3 proportion.

The sinus floor augmentation procedure was performed under local anesthesia using Articaine 4% and epinephrine 1:100 000 (Nova DFL, Rio de Janeiro, Brazil). A crestal incision was made in the maxillary edentulous area, followed by 2 vertical incisions extending both mesial and distal to the lateral sinus wall, as described previously.24,25  A lateral window approach was achieved according to the technique first described by Boyne and James1  (Figure 3a). The mixture of L-PRF and DBBM and the DBBM only were inserted into the respective sinus cavities (Figure 3b and c), and an absorbable collagen membrane was applied to cover the entire obturated lateral window (Figure 3d). The flap was then repositioned and sutured with a nylon thread (Nylon 4-0, Ethicon, Johnson & Johnson, Sao Paulo, Brazil) to achieve primary wound closure.

Figure 3

(a) Clinical procedure for sinus floor augmentation using a lateral window approach. (b) Maxillary sinus filled with a combination of leukocyte and platelet-rich fibrin and Bio-Oss. (c) Only with demineralized bovine bone mineral. (d) Resorbable collagen membrane applied over the graft to avoid epithelial cell migration into the maxillary sinus.

Figure 3

(a) Clinical procedure for sinus floor augmentation using a lateral window approach. (b) Maxillary sinus filled with a combination of leukocyte and platelet-rich fibrin and Bio-Oss. (c) Only with demineralized bovine bone mineral. (d) Resorbable collagen membrane applied over the graft to avoid epithelial cell migration into the maxillary sinus.

Figures 4 and 5.

Figure 4. (a) A new cone-beam computerized tomography (CBCT) image acquisition was taken to evaluate the achieved bone volume in the maxillary sinus. (b) Tridimensional reconstruction image achieved from the CBCT. Figure 5. Final prosthesis delivered after 10 months post-sinus augmentation procedure.

Figures 4 and 5.

Figure 4. (a) A new cone-beam computerized tomography (CBCT) image acquisition was taken to evaluate the achieved bone volume in the maxillary sinus. (b) Tridimensional reconstruction image achieved from the CBCT. Figure 5. Final prosthesis delivered after 10 months post-sinus augmentation procedure.

After surgery, the patient received postoperative instructions for appropriate oral hygiene control, oral antibiotics (amoxicillin, 500 mg 3 times for a week), oral anti-inflammatory (nimesulide, 100 mg 2 times a day for 5 days), and analgesic (paracetamol, 750 mg every 6 hours for 2 days). He was advised to rinse his mouth with chlorhexidine (0.2%) for 14 days. The sutures were removed 10 days after the surgical procedure, and the area was not subjected to any direct loading during the entire bone regeneration phase.

Four months after the sinus augmentation procedure, a new CBCT was taken to evaluate the achieved bone volume (Figure 4a). Based on the tridimensional reconstruction (Figure 4b), 2 dental implants (TitamaxTi EX Acqua 4 × 11 mm, internal exagon, Neodent, Curitiba, Brazil) were planned and installed in the right maxillary sinus and another 6 implants (TitamaxTi EX Acqua 4 × 11 mm; internal exagon, Neodent) were also installed in the upper jaw except on the left sinus. Bone biopsies were harvested from the sinus during implant site preparation with the aid of a 3.0-mm diameter and 10-mm length trephine drill (3i Implant Innovations, Beach Gardens, Fla). After implant placement, the implant stability quotient (ISQ) was measured using an RFA device (Osstell, Integration Diagnostics, Gothenburg, Sweden) in the mesiodistal and buccal-palatal regions, with the mean values used, as described previously.24,26  For the left sinus, 2 dental implants (TitamaxTi EX Acqua 4 × 11 mm; internal exagon, Neodent) were installed after 8 months postsurgical augmentation procedure (4 months after implant installation in the right sinus). Bone biopsies were harvested and RFA analysis was performed, as described above.

Two months after the last surgical technique and 10 months after sinus floor augmentation, prosthetic procedures were carried out to fabricate the definitive prosthesis. This time, implant stability was measured using the RFA apparatus, and the data were recorded. Four and 8 months after the sinus lifting procedure, the augmented bone height was evaluated using volumetric slices achieved with the CBCT scan (SCANORA 3Dx, Soredex, Tuusula, Finland). The parameters used were as follows: 10 mAs, 90 kVp, and a 20-second scan time using the 9-inch field of view. The images were exported to DICOM format and reconstructed using specific software (Planmeca, Roselle, Ill). The analyses were evaluated based on the volumetric dimensions automatically calculated by the software.

Biopsies were immediately fixed in 10% buffered formaldehyde solution for 3 days and then processed, as described elsewhere.25  Serial sections of 6-μm thickness were obtained using an automatic microtome (Jung Supercut 2065, Leica Instruments GmbH, Heidelberg, Germany), mounted on slides, and stained with hematoxylin and eosin. Histological evaluation was made using an optical microscope (Diastar, Leica Microsystems GmbH, Wetzlar, Germany) at ×100 magnification. Images were selected and transferred to a computer display through a digital camera attached to the optical microscope (DFC-300-FX, Leica) allowing histomorphometric analysis in a specific software (Image J 1.45, Wayne Rasband National Institutes of Health, Bethesda, Md). Histomorphometric analysis was performed to measure the newly formed bone, the reminiscent bone graft, and the amount of fibrous tissue after sinus floor augmentation. Selected slides for histomorphometric analysis followed the semi-series standard: The first section of the first slide was selected, then 4 sections sequencing were rejected, and so on.

Clinical Outcomes

During the healing period, the patient did not wear any provisional removable denture. No complications were observed during or after the sinus augmentation procedure. No perforation of the sinus membrane was verified, and none of the implants inserted were lost during the follow-up period. The final prosthesis was delivered 10 months after the sinus augmentation procedure (Figure 5a). CBCT evaluation showed an increased bone resorption in the sinus filled with L-PRF and DBBM compared to the left sinus (22.52% and 8.95%, respectively; Table 1). ISQ were higher than 68 for all implants tested in all the time points (Table 2). Histomorphometric analysis (Figure 6a through d, Table 3) showed higher proportion of newly formed bone in the sinus filled with L-PRF compared to the contralateral side (2 118 102 and 975 535 mm3, respectively). Moreover, the addition of L-PRF allowed a fast healing process, as evidenced by the higher amount of neoformed bone and less fibrous tissue in the sinus, compared to the group without L-PRF (Figure 6a through d). Osseointegration of dental implants installed after 4 months in the right sinus was successfully achieved. Six months after functional loading, stable bone levels were accomplished with the employed protocols.

Table 1

Cone-beam computerize tomography evaluation after sinus floor augmentation in the right (L-PRF + Bio-Oss) and in the left side (Bio-Oss) of the maxillary sinus. Values were obtained in cm3 using the Planmeca software.*

Cone-beam computerize tomography evaluation after sinus floor augmentation in the right (L-PRF + Bio-Oss) and in the left side (Bio-Oss) of the maxillary sinus. Values were obtained in cm3 using the Planmeca software.*
Cone-beam computerize tomography evaluation after sinus floor augmentation in the right (L-PRF + Bio-Oss) and in the left side (Bio-Oss) of the maxillary sinus. Values were obtained in cm3 using the Planmeca software.*
Table 2

Implant stability quotient (ISQ) values measured immediately after implant placement (initial) and before prosthesis installation (final) in the buccal-palatal (B-P) and in the medial-distal (M-D) regions of the implants*

Implant stability quotient (ISQ) values measured immediately after implant placement (initial) and before prosthesis installation (final) in the buccal-palatal (B-P) and in the medial-distal (M-D) regions of the implants*
Implant stability quotient (ISQ) values measured immediately after implant placement (initial) and before prosthesis installation (final) in the buccal-palatal (B-P) and in the medial-distal (M-D) regions of the implants*
Figure 6

Histomorphometric analysis of the bone biopsies harvested during implant site preparation. (a) Bone biopsy collected from the left maxillary sinus filled with only demineralize bovine bone mineral. (b) Representative image from the biopsy in which the blue color represents the newly formed bone, green color is fibrous tissue, and orange color is the bone graft material. (c) Bone biopsy collected from the right sinus. (d) Representative image demonstrating increased amount of newly formed bone (blue color) in the sinus filled with leukocyte and platelet-rich fibrin.

Figure 6

Histomorphometric analysis of the bone biopsies harvested during implant site preparation. (a) Bone biopsy collected from the left maxillary sinus filled with only demineralize bovine bone mineral. (b) Representative image from the biopsy in which the blue color represents the newly formed bone, green color is fibrous tissue, and orange color is the bone graft material. (c) Bone biopsy collected from the right sinus. (d) Representative image demonstrating increased amount of newly formed bone (blue color) in the sinus filled with leukocyte and platelet-rich fibrin.

Table 3

Values of the histological analysis (mm3) evaluating newly formed bone, the amount of bone graft and the fibrous tissue

Values of the histological analysis (mm3) evaluating newly formed bone, the amount of bone graft and the fibrous tissue
Values of the histological analysis (mm3) evaluating newly formed bone, the amount of bone graft and the fibrous tissue

Discussion

The findings of this case report demonstrated that the addition of L-PRF to the DBBM graft on the maxillary sinus did accelerate bone healing, allowing early placement of dental implants (4 months after sinus augmentation compared to the conventional period of 8 months when DBBM is used alone). Moreover, histomorphometric analysis showed a higher amount of newly formed bone (Figure 6c and d) when the growth factor was applied (Table 3). RFA analysis confirmed high ISQ values for the implants installed in both sinus cavities, which represents an adequate implant stability,24,26  immediately after implant placement and before prosthesis installation (Table 2). However, a decrease in bone volume was evidenced by CBCT when L-PRF was added into the sinus (Table 1).

The increased bone resorption in the sinus filled with L-PRF might be explained by compression force during the insertion of the graft in the sinus cavity, surgical technique, or the height of residual bone. Furthermore, a lower amount of DBBM was applied to the sinus when associated with L-PRF. Paralleling clinical data from a previous study,27  the resorption rate when DBBM is used varies between 13.9% and 26% after 6 months postsurgery, which closely resemble our findings. According to a previous study,7  there is no significant relationship between the resorption of grafted bone and the implant success rate (osseointegration) due to the increased stability of the graft over time, especially beyond 12 months postoperative. Indeed, the bone graft in the sinus filled with L-PRF was replaced earlier by newly formed bone, as demonstrated by the blue color in the representative image of the bone biopsy (Figure 6d). Interestingly, the lower amount of graft material used to fill the sinus floor is important to consider when L-PRF is used concomitantly with the graft material. From a practical standpoint, L-PRF is easy to use on the maxillary sinus, and the elastic consistency of the L-PRF membrane allows the clinician to easily insert it inside the sinus floor together with the graft material.

The beneficial effects of L-PRF on tissue healing through release of growth factors, and the enhancement of angiogenesis and osteogenesis might explain the higher amount of newly formed bone in the sinus filled with the combination of bone graft and L-PRF, which are in agreement with a recent systematic review.4  Accordingly, Zhang et al17  compared the association with L-PRF and bovine bone graft with only bovine bone in sinus augmentation. The results showed that the percentage of newly formed bone in the PRF group was higher compared to the control group (18.35 ± 5.62% vs 12.95 ± 5.33%). Further, the percentage of residual graft in the PRF group was about 1.5-fold lower than in the control group (28.54 ± 12.01% vs 19.16 ± 6.89%), which closely resemble our findings. That said, recent studies8,17  have shown that the addition of L-PRF to the DBBM on bone augmentation in maxillary sinus did not increase the percentage of newly formed bone after 6 months postsurgery. Another recent study18  evaluated the efficacy of using L-PRF combined with anorganic bovine bone graft (ABBG; test group) in a 2-stage maxillary sinus augmentation procedure compared to the ABBG alone (control group). The authors showed that there were no differences related to new bone formation when L-PRF was added (35.0 ± 8.6 compared to 32.97 ± 9.71 of control group). Additionally, no differences were noted regarding the amount of connective tissue and biomaterial reminiscent (33.05 ± 6.29 in the test group; 33.79 ± 8.57 in the control group). These findings could be attributed to the differences in the study design, patient characteristics, surgical protocol, healing period, or sample size.

The findings of the present case report suggested that implant placement might be installed earlier than the standard 8 months in grafted areas in the posterior region of the maxilla. Evidently, further longitudinal, randomized, controlled clinical trials are warranted to support this assumption. Similar to this clinical outcome, Choukroun et al28  evaluated the success of PRF and freeze-dried bone allograft (FDBA) mixture for sinus floor augmentation. The authors demonstrated that the combination of L-PRF and FDBA reduced healing time prior to implant installation. They claimed that the healing time could be reduced to 4 months when using PRF, which parallels our findings. According to the authors,28  PRF does not seem to improve cellular proliferation but may play a crucial role in the graft revascularization by supporting angiogenesis and acting as a bio-barrier by protecting the graft material.29  Furthermore, the L-PRF release of growth factors and leukocytes stimulates neoangiogenesis and accelerates tissue healing.

To evaluate the progression of implant stability, RFA was employed immediately after implant placement and before prosthesis installation throughout measurement of the ISQ as a function of firmness of the bone-to-implant interface. Recent observations24,26  have demonstrated that average values of ISQ around 67 represent great implant stability and a complete process of osseointegration. Despite the treatment employed in this case, all implants presented with high ISQ values, demonstrating great implant stability for allowing prosthesis installation. A recent study30  evaluated the effect of L-PRF on bone healing around dental implants installed in the posterior area of the maxilla. ISQ was assessed by RFA 2, 4, and 6 weeks after implant placement. The data showed increased ISQ values when L-PRF was added during surgery for all time points evaluated. The authors suggest that the addition of L-PRF might enhance postinsertion stability of the implants during implant healing. Taken together, the findings presented in this case might suggest the efficacy of L-PRF in accelerating bone healing and allowing early placement of dental implants.

Conclusion

This report demonstrates the advantages of adding L-PRF to the DBBM for maxillary sinus augmentation. The increased new bone formation between these 2 groups (DBBM alone and DBBM + L-PRF) make it possible to consider sinus floor augmentation with a shorter healing period before implant installation (4 months instead of 8 months). Furthermore, the quantity of bone material used to fill the sinus cavity can be safely reduced without compromising the final graft volume. Nevertheless, further longitudinal, prospective, and controlled clinical trials should be performed before justifying the predictability and generalizability for the use of L-PRF and to validate the healing time of 4 months between sinus augmentation and implant installation.

Abbreviations

    Abbreviations
     
  • ABBG

    anorganic bovine bone graft

  •  
  • CBCT

    cone beam computerized tomography

  •  
  • CM

    collagen membrane

  •  
  • DBBM

    demineralized bovine bone mineral

  •  
  • FDBA

    freeze-dried bone allograft

  •  
  • ISQ

    implant stability quotient

  •  
  • L-PRF

    leukocyte- and platelet-rich fibrin

  •  
  • RFA

    resonance frequency analysis

Note

The authors report no conflicts of interest related to this case report.

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