Oral rehabilitation with dental implants has been a successful treatment option for many years. Different implant protocols were developed aiming for safe placement and loading, and faster uncomplicated outcomes.1 Earlier protocols suggested a period of 24–48 weeks for complete healing before the placement of an implant.2 Recently, modified protocols suggest immediate implant placement after tooth extraction. Immediate implant placement minimizes the alveolar bone resorption and lowers the chance of fenestration and dehiscence. Additionally, it reduces the number of surgical sessions and provides better esthetics.3 However, these advantages might be accompanied by minor drawbacks, such as the presence of deficient apical bone and unfavorable postextraction configuration, which might complicate the implant placement and stability. In addition, tension-free suturing might not be feasible when implant placement is accompanied by necessary bone grafting. Furthermore, bur chatter at the osteotomy site might further complicate the situation.4 Therefore, careful patient evaluation and accurate case selection is of utmost importance to provide optimal outcomes.
A gap tends to form at the implant-socket interface when an immediate implant is placed. The dimensions of this gap are influenced by the socket morphology and the implant width and design.5 It was reported that immediate bone healing and osseointegration took place with rough surface implants when a bone-to-implant horizontal defect of ≤2 mm was present.6 Horizontal defects more than 2 mm did not show predictable bone healing.5 Thereafter, guided bone regeneration with different combination protocols have evolved into practice and have shown successful clinical results.7
Collagen membranes appeared as a part of regenerative dentistry in the late 80s, to control soft tissue occlusion and allow the underlying bone to heal.8 Thereafter, collagen membranes became an essential component of ridge augmentation, socket preservation, and guided tissue regeneration.9 A recent preclinical study supported the idea that collagen membranes enhance bone regeneration.10
Recently, Choukroun's platelet-rich fibrin (PRF) was introduced to promote tissue healing in oral-related surgeries.11 Platelet-rich fibrin is a homogenous fibrin biomaterial that is produced simply from autogenous blood samples.12 This concentrate is molded into a membrane form for easier clinical application.13 Platelet-rich fibrin contains different growth factors, such as transforming growth factor-β1 (TGF-β1), platelet-derived growth factor AB (PDGF-AB), vascular endothelial growth factor (VEGF), and matrix glycoprotein thrombospondin-1. Platelet-rich fibrin can continuously release these growth factors for approximately 7 days, in vitro.14 The fibrin mass provides a special biological environment that promotes hemostasis and graft stabilization, and facilitates tissue healing. Additionally, it enhances bone formation and maturation, and makes the handling criteria of the osseous graft material easier. Many studies suggested adding PRF-contained growth factors or platelet-rich plasma (PRP)-derived fibrin glue to the bone graft,13 to further enhance the bone density.15
This study aimed to test if any differences exist between the outcomes of 2 modified immediate implant placement techniques—when slowly resorbable collagen or autogenous PRF membranes are used in the esthetic zone.
Description of the Case
The Declaration of Helsinki on medical protocols and ethics was used to plan and conduct this study at the Oral Surgery Clinic and was approved by the University Ethical Review Board (approval number: 0502018). Fourteen patients were included in this study: 9 males (64.3%) and 5 females (35.7%) with a mean age of 22.54 ± 4.97 years and a range of 18–36 years. These patients came for extraction of a nonrestorable maxillary incisor (Figure 1a) or premolar (Figure 2a) and joined our clinical trial after signing an informed consent. Table 1 shows the demographic information of these patients, restored tooth, implant dimensions, and reason of extraction. All patients agreed to receive an immediate implant, thereafter, they were blindly divided into 2 groups; each contained 7 patients. Ten central incisors (71.4%), 2 lateral incisors (14.3%), and 2 first premolars (14.3%) were replaced by immediate implants. The first group received PRF membranes while the second received collagen membranes and all other treatment components and procedures were the same in both groups. All patients received ceramo-metal crowns and were evaluated at baseline (implant loading time), 6 months, and 12 months postloading.
Inclusion criteria included the presence of the following: adequate horizontal and vertical bone at the future implant site, opposing occlusion, nonsalvageable maxillary incisor or premolar, good oral hygiene, no medical limiting conditions. Exclusion criteria included the presence of the following: teeth adjacent to the future implant that are periodontally or endodontically compromised, no opposing dentition; inadequate oral hygiene and chronic medical conditions, such as hemorrhagic disease or uncontrolled diabetes. Smokers, alcohol abusers, and bruxers were excluded as well.
Two cases are shown in Figures 1 and 2 to outline the technique steps of each treatment group. Each patient was examined comprehensively and a set of panoramic and standardized periapical radiographs (Figures 1b and 2b) and diagnostic models were used to analyze the anatomy and plan for the implant placement. All patients were instructed for oral hygiene and received adequate periodontal scaling prior to implant placement. All implants (100%) were 14 mm in length with different diameters: 3.6 mm (28.6%), 4.0 mm (64.2%), and 4.5 mm (7.2%).
A blood sample was collected from the venous blood of each patient in the first group (n = 7), in a sterile 10 mL-tube (no anticoagulant was added) and centrifuged immediately at 3000 rpm and 400 g for 10 minutes. Platelet-rich fibrin forms between the platelet poor plasma layer at the top of the tube and the red blood cells layer at the bottom of the tube.11 Platelet-rich fibrin membrane (Figure 1c) was prepared at the implant placement time to be used immediately.
A native bilayer of slowly resorbable collagen membrane (Figure 2c; Hypro-Sorb membrane, Bioimplon GmbH) was used for patients assigned to the second group (n = 7). According to the manufacturer, Hypro-Sorb membranes are biphasic bilayer membranes of pure, crystalline atelocollagen (99.9% collagen type I, free of telopeptides) of sterile bovine origin. The membrane was shaped to overlap the extraction socket margins by 2–3 mm and situated to be slightly underneath the marginal mucosa. These placement criteria were suggested to eliminate sharp edges, create a harmonized shape of the augmented area, and minimize bone resorption.16
Under local anesthesia, intrasulcular incision was made to raise a full thickness mucoperiosteal flap and the nonrestorable tooth was atraumatically extracted. Each socket was curetted and irrigated with normal saline to eliminate any residual periodontal ligament or granulation tissue. Drilling for implant placement was set at 600–800 rpm and was performed with a customized surgical guide. Plentiful irrigation was used during drilling steps until the planned dimensions were obtained (Figures 1d and 2d) based on the implant of choice (Dentium System, Superline, Seoul, Korea). Manual key and ratchet were utilized to place the implant. The implant was placed 2–3 mm past the extracted tooth apex to reach better primary stability with the fixture placed 1 mm subcrestal in all cases, and a cover screw was secured to each implant (Figures 1e and 2e).
The remaining space between the implant and the socket was filled in with deproteinized bovine bone mineral (DBBM) (Figures 1f and 2f; Biogen, Xenograft mix, Bioteck S.P.A.) then, either an autogenous PRF membrane (Figure 1g) or a slowly resorbable collagen membrane (Figure 2g) was secured on top of the graft. Directly before flap closure with single stitches (Figures 1h and 2h) of 4.0 silk suture (Supramid, Novaxa Spa), 2 vertical incisions were made to allow for better flap adaptation. Finally, 1 postoperative standardized periapical radiograph was taken for each implant (Figures 1i and 2i).
Amoxicillin 500 mg every 8 hours was prescribed for 1 week to each patient and oral hygiene instructions were reinforced. Patients were advised to eat soft food for 3 days postsurgery and to avoid traumatizing the gingiva at the implant site. Two weeks later, the sutures were removed, and patients presented for evaluation every week for the first 4 weeks after surgery, then, monthly for 12 months after implant loading.
Six months post implant placement and under local anesthesia, a healing abutment replaced each cover screw. After 2 weeks, soft tissue healing was reassessed around the implant and a polyvinyl siloxane impression was taken with a laboratory analogue. The final crown was ready for cementation on the abutment after 1 week (Figures 1j and 2j).
At baseline (implant loading time), 6 months and 12 months postloading, the following parameters were evaluated:
Implant stability using the periotest device (Periotest M, Medizintechnik Gulden).
Modified sulcusbBleedingiIndex (mSBI) was measured at mid-buccal/lingual/mesial/distal sites around each implant.
Peri-implant pocket depth (PPD) was measured at mid-buccal/lingual/mesial/distal sites around each implant.
Standardized periapical radiographs were obtained with the long cone parallel technique, using Rinn XCP (DENTSPLY Friadent Schweiz) film holder and a customized bite-block. Digital tracing of the implant and the alveolar bone was conducted with Scanora 5.2 software program (Tuusula, Finland) for these periapical radiographs. The distance from the implant-abutment connection point to the marginal bone level was recorded, in millimeters. The known implant length, measured from the implant-abutment connection point to the implant apex, was used as a reference, according to the manufacturer's recommendations. A standardized periapical radiograph was taken at each time point for each implant. Figures 1k and 2k show 2 periapical radiographs taken at 12 months (postloading) for a patient from each group.
Numerical data were analyzed for normality with Kolmogorov-Smirnov and Shapiro-Wilk tests. Data are shown as mean ± SD values. Changes within each variable by time were analyzed by Friedman test and pair-wise comparisons were analyzed by Wilcoxon signed-rank test when Friedman test showed significant results. The level of significance was set at P < .05 and the collected data were analyzed with SPSS software (version 20, IBM Corporation). Methodology was reviewed by an independent statistician.
All implants (100%) showed signs of osseointegration and no signs of dehiscence, infection, or mobility. To make results easy to present and interpret, we decided to call the P value (within the same group) of baseline compared with 6 months and 12 months as P1 and to call the P value (within the same group) of 6 months compared with 12 months as P2.
In general, implant stability values (Tables 2 and 3) decreased with time and the difference was not significant between the PRF and collagen groups at baseline, 6 months, and 12 months, respectively. The difference was also insignificant within the PRF group at baseline compared with 6 months and 12 months or at 6 months compared with 12 months. However, it was significant within the collagen group at baseline compared with 6 months and 12 months (P1 < .05) while at 6 months compared with 12 months the difference was insignificant.
No statistical difference in mSBI values was recorded between the 2 groups at baseline, 6 months, and 12 months, respectively (Tables 4–6). No statistical difference of mSBI was found in the PRF group at baseline compared with 6 months and 12 months or at 6 months compared with 12 months, respectively. No bleeding recorded at the palatal site at any time point. In the collagen group, no difference was recorded at baseline compared to 6 months and 12 months or at 6 months compared with 12 months, respectively. No bleeding recorded at the buccal site (at baseline or 6 months) or at the palatal site at any time point.
The difference in PPD was insignificant between the 2 groups at baseline, 6 months and 12 months, respectively (Tables 7–9). The difference of PPD within the PRF group at baseline compared with 6 months and 12 months at the mesial and buccal sites was significant (P < .05) but was insignificant at all other sites. In the collagen membrane group, the difference of PPD was significant at baseline compared with 6 months and 12 months at the distal and buccal sites (P < .05). The difference was not significant at the palatal site at any time point compared with another site or at 6 months compared with 12 months at all other sites.
The standardized periapical radiographs revealed no peri-implant radiolucency. Marginal bone loss (MBL) values of both groups are shown in Tables 10 and 11. In general, MBL values increased in both groups from baseline time to 12 months postloading. No statistical difference was found between the 2 groups at all time points. The difference in PRF group was significant at baseline compared with 6 months and 12-months on mesial and distal sides (P1 < .05), and insignificant at 6 months compared with 12 months. The difference in collagen group at baseline compared with 6 months at the mesial side was significant (P < .05), whereas all other comparisons were insignificant.
This study evaluated the outcomes of immediate implants grafted with DBBM and either an autogenous PRF or a slowly resorbable collagen membrane in the esthetic zone. The 14 implants were loaded after 6 months and were followed up for 12 months postloading. The success rate in our trial was 100% with insignificant changes in the crestal bone level. The small sample size, patients' young age, and strict inclusion criteria might have contributed to this excellent success rate. The biologic advantage of immediate implants is to avoid postsurgical resorption of bone that happens postextraction.17 Immediate implant placement eliminates time wasted for socket compounding, decreases the number of surgeries and reduces the total treatment cost.3
In guided tissue regeneration, membranes with different resorbability were used with or without bone graft for many years to treat periodontal or peri-implant defects.18 However, these membranes are generally expensive and have an increased risk of wound infection. Recently, membranes produced from autogenous blood are becoming more popular.19 Autogenous Choukroun's PRF limits the risk of infection or immune reaction and improves the clotting process and the overall stability of the graft.20 Platelet-rich fibrin releases growth factors for about 7 days, continuously.14 Platelets release some osteogenic cytokines, such as PDGF, VEGF, and insulin-like growth factor (IGF).21 In addition, PRF eliminates the need for using membranes or barriers; hence, reduces the bacterial contamination and its negative impact on the regenerative process.22
In this study, the slowly resorbable collagen membrane provided similar clinical and radiographic outcomes to that of the PRF. A recent preclinical study suggested a promoting role of collagen membrane in guided bone regeneration.10 Kuchler et al23 suggested that the collagen membrane, which serves as a barrier and an osteoconductive scaffold, could possess an osteoinductive role by accumulating growth factors at the surgical site. Growth factors released during tissue healing and regeneration might get adsorbed to this collagen membrane and promote further tissue regeneration. The slowly resorbable collagen membrane used in this study eliminated the need to perform a second surgery to remove the membrane; therefore, it reduced the postsurgical trauma and patient morbidity.24
The use of 2-staged implant technique keeps the implant nonfunctional and reduces the micro-movement during the healing time to facilitate and optimize osseointegration.25 In this trial, the rationale of performing a full thickness mucoperiosteal flap was to facilitate tooth removal and preserve the gingival and mucosal tissues from laceration and subsequent infection. The full thickness flap allows proper inspection of the buccal socket wall for identification of any fenestration or dehiscence, whereas flapless surgery raises perforation risk.26
In this study, the difference in implant stability values was insignificant between both groups at any time point and within the PRF group at different time points but was significant within the collagen group at baseline compared with 6 months and 12 months. Lorenzoni et al27 reported ankylotic healing with successful osseointegration in 100% of their implants. Within the limitations of our trial and the short period of follow up, the recorded periotest values were similar to each other and not sensitive enough to confirm bone turnover or stability changes.27
The mSBI is a clinical indicator of inflammation and no inflammation or suppuration was detected in any of our cases at any time. No statistical difference in mSBI was recorded between the 2 groups at any time point or within each group when compared at different time points. Limited frequency of inflammation could be regarded to the utilization of PRF, which acts like a blood clot—full of growth factors that promotes neoangiogenesis, improves the wound vascularization, and decreases the healing time.22 Similar results were achieved in the collagen membrane group, as collagen might possess an osteoinductive properties along with its known osteoconductive criteria.23
Our PPD results revealed no statistical difference between both groups at any time point. The difference of PPD was significant at the mesial and buccal sites only in the PRF group and the distal and buccal sites only in the collagen group at baseline compared with 6 months and 12 months. Increased incidence of PPD values might be caused by performing a full thickness mucoperiosteal flap, which led to the formation of a more apically positioned junctional epithelium.28 In addition, big open wounds usually heal slowly and show remarkable scar formation that is caused by the impaired vascularity of the mucosa around the implant.29
Marginal bone loss results revealed general increasing values in both groups from baseline time to 12 months postloading; however, the difference between the 2 groups was insignificant at all time points. The difference of MBL in PRF group was significant at baseline compared with 6 months and 12 months on mesial and distal sides, whereas in the collagen membrane group, it was significant between baseline and 6 months at the mesial side only. Bone loss might have resulted from plaque formation that limited bone remodeling around the implant at the time of final prosthesis placement. This possibility might be accompanied by elevated load and consequently high stress levels at the implant-bone connection points.30 In addition, bone loss might have been caused by the subcrestal placement of the implant by 1 mm.31 Bone-to-implant contact ratio was well balanced throughout the follow-up duration. This might be due to the PRF growth factors (PDGF, TGF-β, VEGF, IGF-1), which stimulate angiogenesis, cell proliferation, differentiation, and remodeling. This therapeutic effect enhances faster tissue healing and regeneration at the implant site.21,32 The exact biological mechanism taking place at the surgery site when a resorbable collagen membrane is used is to be verified.
Each patient has a different scenario where the required bone augmentation level varies and anatomical considerations and other systemic conditions might influence the treatment outcomes. Although peri-implant outcomes of this study have added valuable information, additional controlled long-term randomized clinical trials are necessary to confirm the superiority of a treatment technique over another.
Platelet-rich fibrin represent a new technique for activation and hastening of bone regeneration and remodeling. It can be employed as an adjunct to ridge augmentation with immediate implants to benefit patients who require restorations in the esthetic zone, without risk of infection or disease transmission. The outcomes of a slowly resorbable collagen membrane were similar to those of PRF. To date, there are no trials reported to assess the outcomes of using PRF with immediate implant placement or compared this combination to the use of a slowly resorbable collagen membrane. We believe that PRF has the potential to improve the implant bed, motivate osseointegration, and minimize the healing time. This proposed technique requires further evaluation to comparable controls in long-term studies to accurately evaluate the buccal bone wall at the implant site.
deproteinized bovine bone mineral
insulin-like growth factor
marginal bone loss
Modified Sulcus Bleeding Index
peri-implant pocket depth
platelet-derived growth factor AB
transforming growth factor-β1
vascular endothelial growth factor
The authors thank Mansoura University for funding this project and Dr Ahmed Aboulyazid (Assistant Professor at the Faculty of Medicine, Mansoura University) for performing the statistics of this study.
The authors claim no financial interest, either directly or indirectly in the products or information listed in this manuscript.