Skip to main content
Erschienen in:

Open Access 01.12.2023 | Research

The effect of leukocyte- and platelet-rich fibrin on the bone loss and primary stability of implants placed in posterior maxilla: a randomized clinical trial

verfasst von: Meshkat Naeimi Darestani, Hoori Asl Roosta, Seyed Ali Mosaddad, Siamak Yaghoubee

Erschienen in: International Journal of Implant Dentistry | Ausgabe 1/2023

Abstract

Purpose

In this study, we investigated the effects of leukocyte- and platelet-rich fibrin (L-PRF) on implant stability and alterations in the marginal bone surrounding posterior maxillary implants.

Methods

This randomized clinical trial was conducted to compare the variable of L-PRF placement around maxillary implants. Resonance frequency analysis (RFA) was used to evaluate the implant stability immediately after surgery and at 1, 2, 4, 6, 8, and 12 weeks after surgery (t0 to t6, respectively). In addition, the amount of marginal bone changes around the implant at t6 was compared with the baseline using periapical radiography.

Results

The RFA outcomes were statistically significant within each group (P < 0.001, Eta2 = 0.322); however, in none of the follow-ups and immediately after the surgery, there was a significant difference between the two groups in terms of the implant stability quotient (ISQ) scores (P > 0.05). At t0, the test and control groups' respective mean levels of marginal bone loss around the implants were 0.4836 mm and 0.7343 mm, significantly different from the corresponding values at t6. On the other hand, marginal bone loss around the implant was not significantly different between the two groups in t0 and t6 (P = 0.532).

Conclusions

L-PRF did not improve the RFA outcomes of implants three months after implant placement, and changes in the ISQ values over time were the same in both groups. In addition, L-PRF had no superior effect on the marginal bone loss around the implants.
Trial registration number: The research was registered in the Iranian Registry of Clinical Trials on 22 December 2020 (No: IRCT20200624047906N1), available at http://​www.​irct.​ir
Hinweise

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Abkürzungen
L-PRF
Leukocyte- and platelet-rich fibrin
RFA
Resonance frequency analysis
BIC
Bone-to-implant contact
IGF
Insulin-like growth factor
PDGF
Platelet-derived growth factor
BMPs
Bone morphogenic proteins
VEGF
Vascular endothelial growth factor
P-PRP
Pure platelet-rich plasma
L-PRP
Leukocyte and platelet-rich plasma
P-PRF
Pure platelet-rich fibrin
PRP
Platelet-rich plasma
SLA
Sandblasted and acid-etched
ISQ
Implant stability quotient
SD
Standard deviation
ANCOVA
Analysis of covariance
ICC
Intra-class correlation coefficient
PD-ECGF
Platelet-derived endothelial growth factors
FGF-β
Basic fibroblast growth factor
PAF-4
Platelet-activating factor 4
CGF
Concentrated Growth Factor

Background

The primary option for rehabilitating partially or completely edentulous oral cavities is oral implantology [1]. The main prerequisite for the effectiveness of implant therapy is the presence of an adequate bone in the treatment area, both quantitatively and qualitatively, for proper osseointegration [2]. Osseointegration, assessed using the bone-to-implant contact (BIC) value under an optical microscope, refers to direct contact between the bone and the implant [3].
In general, the degree of mineralization, mechanical qualities, and remodeling capability all affect the quality of the bone [4], which is classified into four types, with reducing bone density and strength from type I to type IV [5]. It has been reported that implants' success rate and primary stability in bones with lower qualities (type IV) is lower than that of other bone types [6]. Primary implant stability is the biomechanical stability of implants upon placement. It is controlled by various elements, including the quantity and quality of the bone, the macro/micro design of the implant, the surgical method, and the insertion torque. Following new bone development around the implant's surface over time, biological fixation of the implants to the surrounding bone develops, called secondary implant stability. [7]. Multiple techniques have been recommended to enhance the osseointegration process [8]. According to experimental research, adding molecules or growth factors to the implant surface may increase osteoblastic activity and improve the functional integration of implants [911]. Beneficial growth factors could be delivered to the surface of implants and neighboring bones using platelet derivatives collected from the patient's blood [12, 13]. These derivatives include factors such as insulin-like growth factor (IGF), platelet-derived growth factor (PDGF), bone morphogenic proteins (BMPs), transforming growth factor-β1 (TGF-β1), TGF-β2, and vascular endothelial growth factor (VEGF), to accelerate the healing process and promote differentiation and migration of mesenchymal cells in the area [14].
Platelet derivatives can be divided into four main categories based on leukocyte concentration and fibrin structure. These include pure platelet-rich plasma (P-PRP), leukocyte and platelet-rich plasma (L-PRP), pure platelet-rich fibrin (P-PRF), and leukocyte and platelet-rich fibrin (L-PRF) [12]. Leukocytes and cytokines are present in the second-generation platelet concentrate known as L-PRF, which also has a robust fibrin matrix [15]. Choukroun et al. developed the L-PRF [16], and unlike platelet-rich plasma (PRP), it is produced without the use of anticoagulants [17]. In addition, its procedure generates more significant output volumes and is quicker, cheaper, and less technique-sensitive. Besides, the L-PRF robust fibrin mesh prevents it from disintegrating quickly after application and allows for the progressive release of growth factors improving angiogenesis and osteoblastic proliferation and differentiation [15, 1823]. Various L-PRF indications for oral surgical treatments have been postulated in recent years. One of these treatments involves the application of L-PRF to the implant surface to improve implant stability, followed by improvements in BIC and osseointegration [15]. Another concept is to apply L-PRF over an implant to enhance the thickening of the soft tissues, which would increase the stability of the peri-implant tissues and lessen the loss of marginal bone [24].
Few researchers have examined the impact of PRF on implant stability and bone healing [25, 26]. Due to a fibrin network in PRF, which releases growth factors like PDGF1 and its angiogenesis capacity, the subsequent osteoblastic stimulation is higher in PRF than in PRP [27]. Additionally, PRF is more successful in-vivo than PRP in promoting osteoblastic proliferation and differentiation, which speeds up bone regeneration and fortifies nearby bone by progressively releasing autologous growth factors [27, 28]. With this background in mind, the purpose of this study was to quantitatively investigate the effect of L-PRF on the primary implant stability and to determine the extent of marginal bone changes over time following implant placement in the posterior maxillary regions.

Methods

It was decided to conduct a split-mouth randomized clinical experiment with a 1:1 allocation ratio. Patients referred to the Implant Surgery Department of The Tehran University of Medical Sciences served as the sample source. The Ethics Committee of Tehran University of Medical Sciences authorized the current work (138IR.TUMS.DENTISTRY.REC.1399). Additionally, the research was registered in the Iranian Registry of Clinical Trials at http://​www.​irct.​ir (No: IRCT20200624047906N1). All patients were informed about the specifics of the trial, and everyone gave their written consent before participating.
Based on Tabrizi's study [15] and using the following formula to determine the sample size in clinical trial studies and considering the type I error at 0.05 level and type II error at 0.02 level, the mean (SD) in the intervention group as equal to 88.45 (3.36) and that in the control group as equivalent to 76.15 (2.94), the number of samples for each group was calculated to be 13 and a total of 15 people were included in the study for each group to meet the minimum sample requirement during the study period.
$$n=\frac{( {z}_{1-\frac{\alpha }{2}}+{z}_{1-\beta }{)}^{2}({S}_{1}^{2}+{S}_{2}^{2})}{{({\mu }_{1}+{\mu }_{2})}^{2}}$$
Subjects eligible for inclusion in the study were unilateral or bilateral partially edentulous patients with posterior missing spaces and/or free-end arches requiring dental implants in the maxilla's molars or premolars regions. In the case of unilateral edentulism, both test and control implants were placed on one side of the jaw. Even patients who required more than two maxillary posterior implants, unilaterally or bilaterally, were included in the study. Still, only two of their posterior implants were selected for this study. Patients were screened and chosen based on the inclusion and exclusion criteria listed in Table 1.
Table 1
Patient selection inclusion and exclusion criteria
Inclusion criteria
Exclusion criteria
18 years old (minimum age)
Patients with untreated, periodontal diseases
Systemic health (ASA I, II)
Diabetes or any other metabolic condition that affects bone metabolism
Adequate oral care
Pregnancy or lactation
Stable occlusion
Immunosuppressive drugs or corticosteroids use
Adequate bone height and width at the surgical site (at least 7 mm width and 11 mm height)
History of radiotherapy or chemotherapy
Adequate mesiodistal and interocclusal spaces in the edentulous area
Prior history of sinus lift or bone augmentation
At least six months must have passed following tooth extraction
Primary stability less than 25 Ncm during fixture placement

Preparation of L-PRF

Before surgery, 2 × 10 ml of the patient's venous blood was obtained from the antecubital area and centrifuged symmetrically in glass-coated plastic tubes. The tubes were immediately centrifuged with an IntraSpin machine (Intra-Lock International Inc., Boca Raton, FL, USA) for 12 min at 2700 rpm. Forceps were used to remove the fibrin clot that had developed in the center of the L-PRF tubes. Then, the L-PRF was separated from the red blood cell clot discovered right underneath (Fig. 1a), then transferred to the PRF box (Fig. 1b), and the Xpression tray of the Intraspin system was placed on it. After five minutes, the obtained membrane was ready for use at the surgery site (Fig. 1c).

Surgical method and randomization

All patients underwent surgery by a single surgeon aimed at eliminating operative variables. Local infiltration was injected buccally and palatally at both test and control sites using 2% lidocaine with 1:100,000 epinephrine. Under anesthesia, a crestal incision was made on the desired areas, followed by buccal and palatal full-thickness flap elevation to expose the alveolar crest. Both implantation areas were prepared according to the protocol (25 Ncm, 800 rpm) proposed by the implant manufacturer (Dentium Co., Seoul, Korea).
Random allocation software was used to produce the random sequence. A randomized allocation table was also generated using balanced block randomization. Once the research statistics partner had prepared the randomized allocation list, sealed envelopes numbered sequentially by the practitioner using the letters "T" (indicating the test group) or "C" (meaning the control group) were given to patients before embedding the fixture into the sockets immediately following osteotomy of both implant sockets. Right before placing the implant fixture, the surgeon realized which group (control or test) the surgical site belonged to. Since surgery outcomes were detectable by the patient and the surgeon, there was no possibility of blinding, and only the statistician could be blinded. Control and test sites were chosen entirely randomly using a randomization list.
Next, the L-PRF membrane was wrapped around the fixture (Fig. 1d, e) in the test group and placed at the prepared osteotomy site according to the manufacturer's specifications (Dentium Co., Seoul, Korea). Implants were of similar dimensions (diameter: 4 mm; length: 10 mm) and were inserted in maxillary premolars or molars regions. The implants used in this study were bone-level platform switching Implantium implants (Dentium Co., Seoul, Korea) with a threaded root-form macro design and a sandblasted and acid-etched (SLA) micro design. In the control area, a fixture of the same size was placed without the prior use of L-PRF. Both fixtures were placed 1 mm sub-crestally and then tightened with a torque wrench until both fixtures had reached the desired primary stability (25 Ncm). On both fixtures, a healing abutment was positioned. Using a 4-0 monofilament nylon suture (Supalon, Supa, Iran), the buccal and palatal flaps were re-attached for a passive primary closure. One session was used to operate on each patient. After surgery, all patients were given instructions to use 400 mg of ibuprofen (an NSAID, three times a day for two days), 500 mg of amoxicillin (a systemic antibiotic, three times a day for five days), and 0.2% chlorhexidine mouthwash (twice daily for one week). Two weeks after surgery, all sutures were removed.

Implant stability measurement

The resonance frequency analysis (RFA) technique assessed the implant stability. By attaching its transducer (SmartPeg) to the fixture, the Osstell® device (Osstell, Gothenburg, Sweden) was used to take measurements (Fig. 2a, b). The measurements range from 1 to 100, and a higher number on the implant stability quotient (ISQ) scale denotes a more stable implant. Four buccal, palatal, mesial, and distal ISQs were recorded for each fixture, and the mean value was reported for each implant. The RFA measurements were done right away following the surgery (t0) and repeated one (t1), two (t2), four (t3), six (t4), eight (t5), and 12 weeks (t6) after that. As a graphical abstract, Fig. 3 illustrates the whole procedure performed in this study.

Radiographic evaluation

Immediately after surgery, the placed implants were assessed in all patients employing standardized periapical radiography (KODAK 2100 Intraoral X-Ray System and KODAK RVG 5200 Sensor, Carestream, USA), which was repeated 12 weeks after surgery (t6). To standardize periapical radiographic images, both images were acquired using a film holder (Kerr, Kerr Dental, Switzerland) in a parallel manner. To have the patient close the mouth in a similar pattern at both radiography sessions, a high-viscosity additional silicone putty material (Variotime, Kulzer, Germany) was used for bite registration; it was used to ensure the correct position of the film when acquiring both images. The fixture platform was considered a fixed reference line, and the bone level was defined as the point of greatest coronal contact between the bone and the implant. Finally, the distance between these two points was measured separately for the implants’ mesial and distal sites using ImageJ software (ImageJ, National Institutes of Health, Bethesda, MD, USA) (Fig. 4a, b). In baseline radiographs and those obtained after 12 weeks, the average value of mesial and distal crestal bone changes around the implants was measured and compared. To calibrate the measurements in radiographic images, the implant length and diameter, which were already available, were used for calibration.

Blinding procedure

The patient and surgeon could detect the surgical outcomes, so blinding was not possible. However, during the follow-ups, the assessment clinician who carried out the radiographic examination and the ISQ measurement was unaware of the examined group type (L-PRF or control). Moreover, during data analysis, the statistician who carried out the statistical analyses was unaware of the selective treatment process at each surgical site, and the data analyses were unbiased.

Statistical analysis

The statistical analyses were done using the SPSS software version 19 (SPSS Inc., Chicago, IL, USA). The ISQ changes in the two groups were measured at various intervals and reported as mean and standard deviation (SD). The ISQ changes were compared within each group and between the two groups using a GLM Univariate with Greenhouse–Geisser (Repeated Measure) method. Furthermore, Analysis of covariance (ANCOVA)(general linear model) was used to compare the marginal bone loss around the implants over time between the two groups and within each group based on the results obtained from periapical radiographs. The statistical significance level was set at less than 0.05.

Results

This randomized clinical trial study included 15 patients referred to the periodontology department at Tehran University of Medical Sciences with two or more lost teeth in the posterior maxilla region from December 2020 to June 2021. The trial was terminated when the estimated sample size was reached. Following one patient's withdrawal for personal reasons, there were 14 patients with 28 implants, as shown in Fig. 5. Each test and control group consisted of 7 patients with 14 implants. The patients were 35.7% (n = 5) males and 64.3% (n = 9) females. The average age of patients was 48.93 ± 13.36 years. Table 2 provides an overview of the study participants' demographic characteristics.
Table 2
Demographic characteristics of the research participants in the study groups
 
Test group
Control group
Number of patients
14
14
Number of implants
14
14
Age (years)
48.93 ± 13.36
Gender (Male/Female)
M:5/F:9
M:5/F:9
Maxillary region (Premolar/Molar)
P:11/M:3
P:9/M:5
Smoker
None
None

ISQ changes over time

Table 3 depicts the L-PRF and control groups' mean (SD) of ISQ values over time. The mean ISQ values in the test and control groups were 62.0 ± 10.39 and 61.3 ± 13.04 at t0 (baseline), respectively, and 70.2 ± 7.21 and 70.4 ± 5.29 in the three-month follow-up (t6). Because Mauchly's sphericity assumption was not established Due to the non-establishment of Mauchly's sphericity assumption (P < 0.001), the homogeneity of the variance–covariance matrix was not found, and the Greenhouse–Geisser test results were used. As shown in Fig. 6, the repeated measures test results showed that the intra-group changes in ISQ value were significant over time in both groups (Eta2 = 0.322, P < 0.001). That is, the intra-group differences in ISQ value between t2 and t0 (P = 0.04), t5 and t0 (P = 0.027), and t6 and t0 (P < 0.001) were statistically significant. Nonetheless, there was no significant inter-group interaction effect (P > 0.05). Regarding ISQ value changes over time, the two groups had no significant difference (P = 0.833).
Table 3
Mean (SD) of ISQ values for implants in the intervention and control groups over time
Group
T0
T1
T2
T3
T4
T5
T6
Mean (SD)
Mean (SD)
Mean (SD)
Mean (SD)
Mean (SD)
Mean (SD)
Mean (SD)
L-PRF
62.0 (10.39)
59.5 (8.83)
58.1 (11.30)
58.6 (10.04)
61.7 (10.68)
65.9 (8.89)
70.2 (7.21)
Control
61.3 (13.04)
59.9 (11.56)
58.4 (11.78)
60.8 (7.07)
61.7 (10.25)
67.9 (8.70)
70.4 (5.29)
T Test Group, C Control Group, t time following surgery; t0 (immediately after surgery, t1 (one week), t2 (two weeks), t3 (four weeks), t4 (six weeks), t5 (eight weeks), t6 (12 weeks)

Marginal bone loss

At t0, the mean (SD) of marginal bone loss surrounding the implants in the test and control groups was 0.48 (0.39) and 0.73 (0.62), respectively, which was significantly different from the corresponding values reported at t6 − 0.28 (0.45) and − 0.30 (0.39) in the test and control groups, respectively (P < 0.001) (Table 4). According to descriptive analyses, the mean (standard error) of changes in the studied groups was − 0.340 (0.109) and − 0.240 (0.109), respectively, for the control and the L-PRF groups.
Table 4
Comparison of marginal bone loss at t0 and t6 in the intervention and control groups
Group
Time
Mean
Std. deviation
t
df
Sig. (2-tailed)
Control
T0
.7343
.62052
5.900
13
 < 0.001
T6
−.3004
.39664
L-PRF
T0
.4836
.38957
7.815
13
 < 0.001
T6
− .2796
.45404
The pairwise comparison of marginal bone loss surrounding the implants in both groups was evaluated using an ANCOVA. After 12 weeks, there were no statistically significant differences in the amount of marginal bone loss surrounding the implants between the intervention and control groups (mean difference = − 0.099; 95% CI: − 0.42, 0.22, P = 0.532).

Intra-observer reliability

Ten samples were measured again in radiographic images to ensure the reproducibility of marginal bone surface measurements around the implants. The intra-class correlation coefficient (ICC) index was calculated for two-way random and absolute-agreement models in SPSS. The calculated ICCs were equal to or greater than 0.995.

Discussion

L-PRF is one of the most recent new compounds in the category of platelet derivatives [9, 12]. This concentrate contains high levels of growth factors, such as PDGF1, TGFβ1, TGFβ2, VEGF, platelet-derived endothelial growth factors (PD-ECGF), interleukin-1 (IL-1), IL-2, basic fibroblast growth factor (FGF-β), and platelet-activating factor 4 (PAF-4) [14]. Previous studies have investigated the synergistic role of platelet derivatives in bone and soft tissue healing [2933]. Studies have also examined PRF and its clinical use in several dental fields. PRF treats gingival recessions, periodontal defects, cyst drainage, sinus augmentation, improvement of the width and height of the alveolar bone, ridge preservation, and periodontal defects [9, 3436]. There are, however, few investigations on the effects of PRF use on the quantity and quality of bone surrounding implants; besides, most of these studies had many intervening factors that might have affected the results.
Since the osteoinductive properties of growth factors such as BMPs and TGF-β in bone healing around the implant have been proven, and PRF is also a rich source of these growth factors, what we expect about the use of this material around the implant is increasing implant stability immediately after surgery, accelerating tissue healing and promoting the formation of new bone at the implant site [37, 38]. Since accurate measurement of these parameters is just possible histologically by tissue samples, it would not be possible to definitively determine the type of healing, time, and process of osseointegration around the implant. But, the clinical manifestation of the healing and ossification around the implant usually appears as the stiffness of the BIC, which can be evaluated using RFA [39]. It can also be presented and compared with ISQ quantitative criteria [40]. In addition, it has been suggested that there is a correlation between ISQ values and histological results [41]. Following site preparation for an implant osteotomy, the primary stability is provided by the implant solely through mechanical interaction with the bone. The mechanical stability of the implant is eventually replaced by secondary or biological stability throughout the healing process. The process of contact osteogenesis and the development of peri-implant woven bone to lamellar bone can explain the increase in ISQ values [42, 43]. Accordingly, the current study aimed to assess L-PRF's impact as a bioactive substance on the bone quality and quantity level around the posterior maxillary implants by measuring clinical stability and marginal bone changes with and without using L-PRF. The intervening and bias-causing factors were adjusted as much as possible.
According to the study findings, the two groups had no significant difference in implant stability. The trend of ISQ changes remained relatively stable over time for the implants in both groups after three months. Additionally, there were no discernible differences between the groups during the three-month follow-up regarding the impact of the L-PRF membrane on marginal bone loss around the implants.
These results contradict the findings of a study by Öncü et al., which investigated the effect of L-PRF on the initial stability of the implant and hard tissue healing. Their results indicated the positive impact of L-PRF on ISQ in one and four-week intervals [25]. The differences between the Öncü study and our study can justify the discrepancy in the data; the implants in that study were all placed in type I and II mandibular bone. Of course, several studies have stated that ISQ values differ for maxillary and mandibular implants [4447]. Also, the follow-up period in the Öncü study was only one month as it is evident that about one month after the implant placement, the surrounding bone is in the osteoclastic phase, and the implant's stability shows a significant drop compared to the surgical time [48]. A systematic review found that using L-PRF improved implant stability after one week and four weeks, but the difference immediately after insertion was not statistically significant [37].
In the present study, according to the RFA reports, implants in both groups showed descending and ascending trends in the ISQ values over time. The effects of L-PRF on improving stability were insignificant. The L-PRF membrane appears to have been resorbed before causing bone changes around the implant. Since the placement of the L-PRF membrane was done on the fixture when the fixture entered the osteotomized socket, the implant threads first engage with the L-PRF membrane and then with the bone walls, and some of the extra volumes of L-PRF come out of the socket after the complete placement of the fixture. Therefore, the L-PRF membrane remains between the fixture and the bone. Considering that the L-PRF is resorbed about two weeks later [49], it is expected that with the dislodgement of the L-PRF membrane, there will be a micro-gap between the bone and the fixture. During this time, the osteogenic cells have not yet had the opportunity to ossify and fill this micro-gap; on the contrary, the surrounding bone enters the osteoclastic phase, and the implant's stability at this stage is much less than immediately after surgery. Together, these two factors have resulted in the recorded ISQ of the test group implants being lower than that of the control group throughout this time. Finally, after passing this period, we can see that the ISQ values of the implants of both groups have increased over time.
PRP significantly boosted the stability of dental implants within 12 weeks of placement, according to a study by Quesada-Garca et al. [50]. However, there were many intervening factors in the study mentioned above, including patient-related and implant-related variables. In addition, growth factors in plasma were used instead of L-PRF membrane on the surfaces of the implants. On the other hand, research by Ergun et al. and Monov et al. revealed that growth factors high in platelets have no discernible effects on osseointegration [51, 52].
According to the present study, after 12 weeks, the stability of both test and control groups was reported at the same level. This could be due to the limitation of the interfering factors in our study and the split-mouth design for selecting samples. In a study performed by Kapoor et al. [53], between baseline and three months, there was a highly significant rise in ISQ scores in both the PRF and control groups. Our results also agree with this study and another by Diana et al. [54], who also discovered a significant improvement in implant stability over three months in both PRF and control groups. However, there was no significant difference between the groups. A systematic review showed that PRF provided little to no benefit in treating peri-implantitis, implant stability, or guided bone regeneration, as tested in numerous trials [55].
With all these findings, using L-PRF around immediate implants after tooth extraction can be justified; in a previous animal study with a split-mouth design, L-PRF impact on osseointegration around immediate implants in the mandible was compared with a control group [56]. In histological analysis, they confirmed the favorable effect of L-PRF on osteogenesis around implants. It was also reported that in the group which did not have L-PRF to fill the gap between the implant and the extraction socket walls, the apical growth of soft tissue was observed, and the rate of ossification was lower than the L-PRF group. This study suggested that L-PRF could be used as an optimal autogenic source to fill the gap between the extraction socket walls and the implant while improving osseointegration and preventing soft tissue apical growth in the socket; it was also absorbed and removed from the site. Therefore, it did not interfere with the natural process of ossification; the significant difference with our study was the time of implantation and the existing gap between the implant and the bone augmented by L-PRF. The study above justifies the efficiency of using L-PRF in fresh socket implants [56] because the role of L-PRF as a scaffold in the gap is much more vital than its biological properties. In implants placed immediately, the gap between the extraction socket walls and the implant is left alone. Ideally, the blood clot between the implant and the bony wall creates a bone tissue in which the osseous cells may migrate from the socket margin to its center for intramembranous ossification., but after the shrinkage of the clot and its separation from the surface of the fixture, the growth of soft tissue has occurred towards the inside of the cavity disrupting the connection of the clot and bone-forming cells with the implant [57]. As reported, the L-PRF acted as a physical barrier in the area [17, 58], preventing the down growth of soft tissue into the socket. Thus the opportunity for soft tissue intervention in bone repair has been denied. This justification agrees with the results obtained from the study of Benalcázar et al. [59]; the study demonstrated that before implantation, L-PRF placement within wide osteotomies led to increased early bone growth as compared to unfilled wide osteotomies at the early healing time (three weeks in-vivo). In our study, the delayed placement of implants eliminated the need for scaffolding and physical barriers.
In a prospective cohort study conducted by Özveri et al. [60], the use of concentrated growth factor (CGF) around the implant was investigated, and the numerical stability of the implant during surgery and intervals of 1, 2, and 4 weeks was reported by RFA. The study findings showed that CGF does not improve implant stability during the initial healing phase. In an RCT study performed by Gaur et al. [61], three groups (control, PRF, and CGF) were investigated by comparing the stability of immediately placed dental implants using RFA and the bone regeneration around them by measuring radiodensity and the bone gap (horizontal/vertical) on periapical images over time. In agreement with our study, although intergroup results were not significant at any time, they concluded that the treatment of platelet concentrates appeared to improve implant stability. Comparing the quantity (horizontal and vertical gap reduction) and quality (radiodensity/grayscale) of bone regeneration across the three groups showed no statistically significant difference.
In another study by Tabrizi et al. in 2018 on the effect of L-PRF membranes around implants on clinical stability, it was found that the L-PRF membranes could improve the ISQ values of implants during six weeks of follow-up compared to the control group [15]. It should be noted that their follow-up study was shorter than ours, and the results of these studies were even contradictory in six weeks. Among the reasons that may justify the lack of statistically significant difference between the ISQ values of the implants in the test and control groups in our study, we can mention the proximity of the two implants in some patients. Almost in half of the samples of our study, the implants of the test and control groups were located on the same posterior side of the upper jaw, and considering that after the enzymatic breakdown of the L-PRF membrane, fibrinopeptides are used in different ways by the cells in the area around the defect. The breakdown products can apply effective promotional effects locally in the defect and surrounding areas [62, 63]. Therefore, the possibility of unintentionally affecting the implants of the control group from the intervention carried out for the implants of the test group located in the vicinity should also be considered.
In two studies by Kundu et al. [34] and Boora et al. [24] on marginal bone changes around implants associated with L-PRF placement, marginal bone loss around implants was not affected by L-PRF [24, 34]. Moreover, the study by Kundu et al. [34] concluded that implant stability was positively impacted by PRP only at baseline and that there was no significant difference between the two groups in subsequent analyses. In this regard, a systematic review revealed that in the short term, platelet concentrates could considerably increase implant stability and lessen marginal bone loss [64].
Overall, the regional acceleratory phenomenon during drilling and implantation seems sufficient to initiate osteogenesis and induce the growth and differentiation of bone stem cells around implants. Within the limitations of this study, the addition of L-PRF by increasing the dose of growth factors cannot further stimulate osteoprogenitor cells to improve and accelerate ossification. There is probably a physiological range for the induction of cell growth and differentiation by growth and inflammatory factors, which is not limitless or dose-dependent. Therefore, despite all its benefits, L-PRF might not have any additive effects on bone repair around implants. However, large-scale studies with prolonged follow-up periods are still needed to draw firm conclusions.

Conclusions

In light of the present study's shortcomings, it could be stated that compared to the control group, applying L-PRF did not improve the RFA outcomes in the posterior maxilla three months after implant insertion. Changes in the ISQ values over time were similar in the two groups, and the interaction was not affected by using L-PRF. Besides, the rate of marginal bone loss around the implant was not significantly affected by L-PRF.

Acknowledgements

This investigation is based on a post-graduate thesis at Tehran University of Medical Sciences, School of Dentistry, Periodontics Department. We appreciate the financial support for this work provided by Dr. Ahmadreza Shamshiri, Vice-Chancellor for Research at Tehran University of Medical Sciences, School of Dentistry.

Declarations

The Ethics Committee of Tehran University of Medical Sciences authorized the current work (138IR.TUMS.DENTISTRY.REC.1399). All patients involved in the study were informed about the specifics of the trial, and everyone gave their written permission before participating.
Not applicable.

Competing interests

The authors have no competing interests.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://​creativecommons.​org/​licenses/​by/​4.​0/​.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Literatur
1.
Zurück zum Zitat Alghamdi HS. Methods to improve osseointegration of dental implants in low quality (Type-IV) bone: an overview. J Funct Biomater. 2018;9(1):7.PubMedPubMedCentral Alghamdi HS. Methods to improve osseointegration of dental implants in low quality (Type-IV) bone: an overview. J Funct Biomater. 2018;9(1):7.PubMedPubMedCentral
2.
3.
Zurück zum Zitat Hao C-P, Cao N-J, Zhu Y-H, Wang W. The osseointegration and stability of dental implants with different surface treatments in animal models: a network meta-analysis. Sci Rep. 2021;11(1):13849.PubMedPubMedCentral Hao C-P, Cao N-J, Zhu Y-H, Wang W. The osseointegration and stability of dental implants with different surface treatments in animal models: a network meta-analysis. Sci Rep. 2021;11(1):13849.PubMedPubMedCentral
4.
Zurück zum Zitat Shapurian T, Damoulis PD, Reiser GM, Griffin TJ, Rand WM. Quantitative evaluation of bone density using the Hounsfield index. Int J Oral Maxillofac Implants. 2006;21(2):290–7.PubMed Shapurian T, Damoulis PD, Reiser GM, Griffin TJ, Rand WM. Quantitative evaluation of bone density using the Hounsfield index. Int J Oral Maxillofac Implants. 2006;21(2):290–7.PubMed
5.
Zurück zum Zitat Anitua E, Alkhraisat MH, Piñas L, Orive G. Efficacy of biologically guided implant site preparation to obtain adequate primary implant stability. Ann Anat. 2015;199:9–15.PubMed Anitua E, Alkhraisat MH, Piñas L, Orive G. Efficacy of biologically guided implant site preparation to obtain adequate primary implant stability. Ann Anat. 2015;199:9–15.PubMed
6.
Zurück zum Zitat Degidi M, Piattelli A, Gehrke P, Felice P, Carinci F. Five-year outcome of 111 immediate nonfunctional single restorations. J Oral Implantol. 2006;32(6):277–85.PubMed Degidi M, Piattelli A, Gehrke P, Felice P, Carinci F. Five-year outcome of 111 immediate nonfunctional single restorations. J Oral Implantol. 2006;32(6):277–85.PubMed
7.
Zurück zum Zitat Cobo-Vázquez C, Reininger D, Molinero-Mourelle P, González-Serrano J, Guisado-Moya B, López-Quiles J. Effect of the lack of primary stability in the survival of dental implants. J Clin Exp Dent. 2018;10(1):e14–9.PubMedPubMedCentral Cobo-Vázquez C, Reininger D, Molinero-Mourelle P, González-Serrano J, Guisado-Moya B, López-Quiles J. Effect of the lack of primary stability in the survival of dental implants. J Clin Exp Dent. 2018;10(1):e14–9.PubMedPubMedCentral
8.
Zurück zum Zitat Inchingolo F, Ballini A, Cagiano R, Inchingolo A, Serafini M, De Benedittis M, et al. Immediately loaded dental implants bioactivated with platelet-rich plasma (PRP) placed in maxillary and mandibular region. Clin Ter. 2015;166(3):e146–52.PubMed Inchingolo F, Ballini A, Cagiano R, Inchingolo A, Serafini M, De Benedittis M, et al. Immediately loaded dental implants bioactivated with platelet-rich plasma (PRP) placed in maxillary and mandibular region. Clin Ter. 2015;166(3):e146–52.PubMed
9.
Zurück zum Zitat Choukroun J, Diss A, Simonpieri A, Girard MO, Schoeffler C, Dohan SL, et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part IV: clinical effects on tissue healing. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;101(3):e56-60.PubMed Choukroun J, Diss A, Simonpieri A, Girard MO, Schoeffler C, Dohan SL, et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part IV: clinical effects on tissue healing. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;101(3):e56-60.PubMed
10.
Zurück zum Zitat Zhang C, Zhang T, Geng T, Wang X, Lin K, Wang P. Dental implants loaded with bioactive agents promote osseointegration in osteoporosis: a review. Front Bioeng Biotechnol. 2021;9: 591796.PubMedPubMedCentral Zhang C, Zhang T, Geng T, Wang X, Lin K, Wang P. Dental implants loaded with bioactive agents promote osseointegration in osteoporosis: a review. Front Bioeng Biotechnol. 2021;9: 591796.PubMedPubMedCentral
11.
Zurück zum Zitat Kligman S, Ren Z, Chung CH, Perillo MA, Chang YC, Koo H, et al. The Impact of Dental Implant Surface Modifications on Osseointegration and Biofilm Formation. J Clin Med. 2021;10(8):1641.PubMedPubMedCentral Kligman S, Ren Z, Chung CH, Perillo MA, Chang YC, Koo H, et al. The Impact of Dental Implant Surface Modifications on Osseointegration and Biofilm Formation. J Clin Med. 2021;10(8):1641.PubMedPubMedCentral
12.
Zurück zum Zitat Dohan DM, Choukroun J, Diss A, Dohan SL, Dohan AJ, Mouhyi J, et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part II: platelet-related biologic features. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;101(3):e45-50.PubMed Dohan DM, Choukroun J, Diss A, Dohan SL, Dohan AJ, Mouhyi J, et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part II: platelet-related biologic features. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;101(3):e45-50.PubMed
13.
Zurück zum Zitat Giusti I, D’Ascenzo S, Macchiarelli G, Dolo V. In vitro evidence supporting applications of platelet derivatives in regenerative medicine. Blood Transfus. 2020;18(2):117–29.PubMedPubMedCentral Giusti I, D’Ascenzo S, Macchiarelli G, Dolo V. In vitro evidence supporting applications of platelet derivatives in regenerative medicine. Blood Transfus. 2020;18(2):117–29.PubMedPubMedCentral
14.
Zurück zum Zitat Vijayalakshmi R, Rajmohan CS, Deepalakshmi D, Sivakami G. Use of platelet rich fibrin in a fenestration defect around an implant. J Indian Soc Periodontol. 2012;16(1):108–12.PubMedPubMedCentral Vijayalakshmi R, Rajmohan CS, Deepalakshmi D, Sivakami G. Use of platelet rich fibrin in a fenestration defect around an implant. J Indian Soc Periodontol. 2012;16(1):108–12.PubMedPubMedCentral
15.
Zurück zum Zitat Tabrizi R, Arabion H, Karagah T. Does platelet-rich fibrin increase the stability of implants in the posterior of the maxilla? A split-mouth randomized clinical trial. Int J Oral Maxillofac Surg. 2018;47(5):672–5.PubMed Tabrizi R, Arabion H, Karagah T. Does platelet-rich fibrin increase the stability of implants in the posterior of the maxilla? A split-mouth randomized clinical trial. Int J Oral Maxillofac Surg. 2018;47(5):672–5.PubMed
16.
Zurück zum Zitat Choukroun J, Adda F, Schoeffler C, Vervelle A, editors. Une opportunite´ en paro-implantologie: Le PRF2001. Choukroun J, Adda F, Schoeffler C, Vervelle A, editors. Une opportunite´ en paro-implantologie: Le PRF2001.
17.
Zurück zum Zitat Dohan Ehrenfest DM, Rasmusson L, Albrektsson T. Classification of platelet concentrates: from pure platelet-rich plasma (P-PRP) to leucocyte- and platelet-rich fibrin (L-PRF). Trends Biotechnol. 2009;27(3):158–67.PubMed Dohan Ehrenfest DM, Rasmusson L, Albrektsson T. Classification of platelet concentrates: from pure platelet-rich plasma (P-PRP) to leucocyte- and platelet-rich fibrin (L-PRF). Trends Biotechnol. 2009;27(3):158–67.PubMed
18.
Zurück zum Zitat Dohan Ehrenfest DM, Bielecki T, Mishra A, Borzini P, Inchingolo F, Sammartino G, et al. In search of a consensus terminology in the field of platelet concentrates for surgical use: platelet-rich plasma (PRP), platelet-rich fibrin (PRF), fibrin gel polymerization and leukocytes. Curr Pharm Biotechnol. 2012;13(7):1131–7.PubMed Dohan Ehrenfest DM, Bielecki T, Mishra A, Borzini P, Inchingolo F, Sammartino G, et al. In search of a consensus terminology in the field of platelet concentrates for surgical use: platelet-rich plasma (PRP), platelet-rich fibrin (PRF), fibrin gel polymerization and leukocytes. Curr Pharm Biotechnol. 2012;13(7):1131–7.PubMed
19.
Zurück zum Zitat Sumida R, Maeda T, Kawahara I, Yusa J, Kato Y. Platelet-rich fibrin increases the osteoprotegerin/receptor activator of nuclear factor-κB ligand ratio in osteoblasts. Exp Ther Med. 2019;18(1):358–65.PubMedPubMedCentral Sumida R, Maeda T, Kawahara I, Yusa J, Kato Y. Platelet-rich fibrin increases the osteoprotegerin/receptor activator of nuclear factor-κB ligand ratio in osteoblasts. Exp Ther Med. 2019;18(1):358–65.PubMedPubMedCentral
20.
Zurück zum Zitat Kosmidis K, Ehsan K, Pitzurra L, Loos B, Jansen I. An in vitro study into three different PRF preparations for osteogenesis potential. J Periodontal Res. 2023;58(3):483–92.PubMed Kosmidis K, Ehsan K, Pitzurra L, Loos B, Jansen I. An in vitro study into three different PRF preparations for osteogenesis potential. J Periodontal Res. 2023;58(3):483–92.PubMed
21.
Zurück zum Zitat Wang J, Sun Y, Liu Y, Yu J, Sun X, Wang L, et al. Effects of platelet-rich fibrin on osteogenic differentiation of Schneiderian membrane derived mesenchymal stem cells and bone formation in maxillary sinus. Cell Commun Signal. 2022;20(1):88.PubMedPubMedCentral Wang J, Sun Y, Liu Y, Yu J, Sun X, Wang L, et al. Effects of platelet-rich fibrin on osteogenic differentiation of Schneiderian membrane derived mesenchymal stem cells and bone formation in maxillary sinus. Cell Commun Signal. 2022;20(1):88.PubMedPubMedCentral
22.
Zurück zum Zitat Ratajczak J, Vangansewinkel T, Gervois P, Merckx G, Hilkens P, Quirynen M, et al. Angiogenic properties of “leukocyte- and platelet-rich fibrin.” Sci Rep. 2018;8(1):14632.PubMedPubMedCentral Ratajczak J, Vangansewinkel T, Gervois P, Merckx G, Hilkens P, Quirynen M, et al. Angiogenic properties of “leukocyte- and platelet-rich fibrin.” Sci Rep. 2018;8(1):14632.PubMedPubMedCentral
23.
Zurück zum Zitat Dohle E, El Bagdadi K, Sader R, Choukroun J, James Kirkpatrick C, Ghanaati S. Platelet-rich fibrin-based matrices to improve angiogenesis in an in vitro co-culture model for bone tissue engineering. J Tissue Eng Regen Med. 2018;12(3):598–610.PubMed Dohle E, El Bagdadi K, Sader R, Choukroun J, James Kirkpatrick C, Ghanaati S. Platelet-rich fibrin-based matrices to improve angiogenesis in an in vitro co-culture model for bone tissue engineering. J Tissue Eng Regen Med. 2018;12(3):598–610.PubMed
24.
Zurück zum Zitat Boora P, Rathee M, Bhoria M. Effect of Platelet Rich Fibrin (PRF) on Peri-implant soft tissue and crestal bone in one-stage implant placement: a randomized controlled trial. J Clin Diagn Res. 2015;9(4):Zc18–21. Boora P, Rathee M, Bhoria M. Effect of Platelet Rich Fibrin (PRF) on Peri-implant soft tissue and crestal bone in one-stage implant placement: a randomized controlled trial. J Clin Diagn Res. 2015;9(4):Zc18–21.
25.
Zurück zum Zitat Öncü E, Alaaddinoğlu EE. The effect of platelet-rich fibrin on implant stability. Int J Oral Maxillofac Implants. 2015;30(3):578–82.PubMed Öncü E, Alaaddinoğlu EE. The effect of platelet-rich fibrin on implant stability. Int J Oral Maxillofac Implants. 2015;30(3):578–82.PubMed
26.
Zurück zum Zitat Ortolani E, Guerriero M, Coli A, Di Giannuario A, Minniti G, Polimeni A. Effect of PDGF, IGF-1 and PRP on the implant osseointegration. An histological and immunohistochemical study in rabbits. Ann Stomatol Roma. 2014;5(2):66–8.PubMedPubMedCentral Ortolani E, Guerriero M, Coli A, Di Giannuario A, Minniti G, Polimeni A. Effect of PDGF, IGF-1 and PRP on the implant osseointegration. An histological and immunohistochemical study in rabbits. Ann Stomatol Roma. 2014;5(2):66–8.PubMedPubMedCentral
27.
Zurück zum Zitat He L, Lin Y, Hu X, Zhang Y, Wu H. A comparative study of platelet-rich fibrin (PRF) and platelet-rich plasma (PRP) on the effect of proliferation and differentiation of rat osteoblasts in vitro. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2009;108(5):707–13.PubMed He L, Lin Y, Hu X, Zhang Y, Wu H. A comparative study of platelet-rich fibrin (PRF) and platelet-rich plasma (PRP) on the effect of proliferation and differentiation of rat osteoblasts in vitro. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2009;108(5):707–13.PubMed
28.
Zurück zum Zitat Anitua E, Orive G, Pla R, Roman P, Serrano V, Andía I. The effects of PRGF on bone regeneration and on titanium implant osseointegration in goats: a histologic and histomorphometric study. J Biomed Mater Res A. 2009;91(1):158–65.PubMed Anitua E, Orive G, Pla R, Roman P, Serrano V, Andía I. The effects of PRGF on bone regeneration and on titanium implant osseointegration in goats: a histologic and histomorphometric study. J Biomed Mater Res A. 2009;91(1):158–65.PubMed
30.
Zurück zum Zitat Giudice A, Esposito M, Bennardo F, Brancaccio Y, Buti J, Fortunato L. Dental extractions for patients on oral antiplatelet: a within-person randomised controlled trial comparing haemostatic plugs, advanced-platelet-rich fibrin (A-PRF+) plugs, leukocyte- and platelet-rich fibrin (L-PRF) plugs and suturing alone. Int J Oral Implantol (Berl). 2019;12(1):77–87.PubMed Giudice A, Esposito M, Bennardo F, Brancaccio Y, Buti J, Fortunato L. Dental extractions for patients on oral antiplatelet: a within-person randomised controlled trial comparing haemostatic plugs, advanced-platelet-rich fibrin (A-PRF+) plugs, leukocyte- and platelet-rich fibrin (L-PRF) plugs and suturing alone. Int J Oral Implantol (Berl). 2019;12(1):77–87.PubMed
31.
Zurück zum Zitat Dragonas P, Katsaros T, Avila-Ortiz G, Chambrone L, Schiavo JH, Palaiologou A. Effects of leukocyte-platelet-rich fibrin (L-PRF) in different intraoral bone grafting procedures: a systematic review. Int J Oral Maxillofac Surg. 2019;48(2):250–62.PubMed Dragonas P, Katsaros T, Avila-Ortiz G, Chambrone L, Schiavo JH, Palaiologou A. Effects of leukocyte-platelet-rich fibrin (L-PRF) in different intraoral bone grafting procedures: a systematic review. Int J Oral Maxillofac Surg. 2019;48(2):250–62.PubMed
32.
Zurück zum Zitat Pichotano EC, de Molon RS, de Souza RV, Austin RS, Marcantonio E, Zandim-Barcelos DL. Evaluation of L-PRF combined with deproteinized bovine bone mineral for early implant placement after maxillary sinus augmentation: a randomized clinical trial. Clin Implant Dent Relat Res. 2019;21(2):253–62.PubMed Pichotano EC, de Molon RS, de Souza RV, Austin RS, Marcantonio E, Zandim-Barcelos DL. Evaluation of L-PRF combined with deproteinized bovine bone mineral for early implant placement after maxillary sinus augmentation: a randomized clinical trial. Clin Implant Dent Relat Res. 2019;21(2):253–62.PubMed
33.
Zurück zum Zitat Temmerman A, Cleeren GJ, Castro AB, Teughels W, Quirynen M. L-PRF for increasing the width of keratinized mucosa around implants: a split-mouth, randomized, controlled pilot clinical trial. J Periodontal Res. 2018;53(5):793–800.PubMed Temmerman A, Cleeren GJ, Castro AB, Teughels W, Quirynen M. L-PRF for increasing the width of keratinized mucosa around implants: a split-mouth, randomized, controlled pilot clinical trial. J Periodontal Res. 2018;53(5):793–800.PubMed
34.
Zurück zum Zitat Kundu R, Rathee M. Effect of platelet-rich-plasma (PRP) and implant surface topography on implant stability and bone. JCDR. 2014;8(6):ZC26-ZC30. Kundu R, Rathee M. Effect of platelet-rich-plasma (PRP) and implant surface topography on implant stability and bone. JCDR. 2014;8(6):ZC26-ZC30.
35.
Zurück zum Zitat Aroca S, Keglevich T, Barbieri B, Gera I, Etienne D. Clinical evaluation of a modified coronally advanced flap alone or in combination with a platelet-rich fibrin membrane for the treatment of adjacent multiple gingival recessions: a 6-month study. J Periodontol. 2009;80(2):244–52.PubMed Aroca S, Keglevich T, Barbieri B, Gera I, Etienne D. Clinical evaluation of a modified coronally advanced flap alone or in combination with a platelet-rich fibrin membrane for the treatment of adjacent multiple gingival recessions: a 6-month study. J Periodontol. 2009;80(2):244–52.PubMed
36.
Zurück zum Zitat Ziyad SH. L-PRF: A “Super” Biomaterial for Naturally Guided Hard/Soft Tissue Bioengineering and Regeneration of Oro-Dental, Periodontal and Jaw Defects. In: Raja K, editor. Bone Grafting. Rijeka: IntechOpen; 2018. p. Ch. 8. Ziyad SH. L-PRF: A “Super” Biomaterial for Naturally Guided Hard/Soft Tissue Bioengineering and Regeneration of Oro-Dental, Periodontal and Jaw Defects. In: Raja K, editor. Bone Grafting. Rijeka: IntechOpen; 2018. p. Ch. 8.
37.
Zurück zum Zitat Lyris V, Millen C, Besi E, Pace-Balzan A. Effect of leukocyte and platelet rich fibrin (L-PRF) on stability of dental implants. A systematic review and meta-analysis. Br J Oral Maxillofac Surg. 2021;59(10):1130–9.PubMed Lyris V, Millen C, Besi E, Pace-Balzan A. Effect of leukocyte and platelet rich fibrin (L-PRF) on stability of dental implants. A systematic review and meta-analysis. Br J Oral Maxillofac Surg. 2021;59(10):1130–9.PubMed
38.
Zurück zum Zitat Guan S, Xiao T, Bai J, Ning C, Zhang X, Yang L, et al. Clinical application of platelet-rich fibrin to enhance dental implant stability: A systematic review and meta-analysis. Heliyon. 2023;9(2): e13196.PubMedPubMedCentral Guan S, Xiao T, Bai J, Ning C, Zhang X, Yang L, et al. Clinical application of platelet-rich fibrin to enhance dental implant stability: A systematic review and meta-analysis. Heliyon. 2023;9(2): e13196.PubMedPubMedCentral
39.
Zurück zum Zitat Degidi M, Perrotti V, Piattelli A, Iezzi G. Mineralized bone-implant contact and implant stability quotient in 16 human implants retrieved after early healing periods: a histologic and histomorphometric evaluation. Int J Oral Maxillofac Implants. 2010;25(1):45–8.PubMed Degidi M, Perrotti V, Piattelli A, Iezzi G. Mineralized bone-implant contact and implant stability quotient in 16 human implants retrieved after early healing periods: a histologic and histomorphometric evaluation. Int J Oral Maxillofac Implants. 2010;25(1):45–8.PubMed
40.
Zurück zum Zitat Açil Y, Sievers J, Gülses A, Ayna M, Wiltfang J, Terheyden H. Correlation between resonance frequency, insertion torque and bone-implant contact in self-cutting threaded implants. Odontology. 2017;105(3):347–53.PubMed Açil Y, Sievers J, Gülses A, Ayna M, Wiltfang J, Terheyden H. Correlation between resonance frequency, insertion torque and bone-implant contact in self-cutting threaded implants. Odontology. 2017;105(3):347–53.PubMed
41.
Zurück zum Zitat Gedrange T, Hietschold V, Mai R, Wolf P, Nicklisch M, Harzer W. An evaluation of resonance frequency analysis for the determination of the primary stability of orthodontic palatal implants. A study in human cadavers. Clin Oral Implants Res. 2005;16(4):425–31.PubMed Gedrange T, Hietschold V, Mai R, Wolf P, Nicklisch M, Harzer W. An evaluation of resonance frequency analysis for the determination of the primary stability of orthodontic palatal implants. A study in human cadavers. Clin Oral Implants Res. 2005;16(4):425–31.PubMed
42.
Zurück zum Zitat Abrahamsson I, Berglundh T, Linder E, Lang NP, Lindhe J. Early bone formation adjacent to rough and turned endosseous implant surfaces. An experimental study in the dog. Clin Oral Implants Res. 2004;15(4):381–92.PubMed Abrahamsson I, Berglundh T, Linder E, Lang NP, Lindhe J. Early bone formation adjacent to rough and turned endosseous implant surfaces. An experimental study in the dog. Clin Oral Implants Res. 2004;15(4):381–92.PubMed
43.
Zurück zum Zitat Sadeghi R, Rokn AR, Miremadi A. Comparison of implant stability using resonance frequency analysis: osteotome versus conventional drilling. J Dent (Tehran). 2015;12(9):647–54.PubMed Sadeghi R, Rokn AR, Miremadi A. Comparison of implant stability using resonance frequency analysis: osteotome versus conventional drilling. J Dent (Tehran). 2015;12(9):647–54.PubMed
44.
Zurück zum Zitat Balleri P, Cozzolino A, Ghelli L, Momicchioli G, Varriale A. Stability measurements of osseointegrated implants using Osstell in partially edentulous jaws after 1 year of loading: a pilot study. Clin Implant Dent Relat Res. 2002;4(3):128–32.PubMed Balleri P, Cozzolino A, Ghelli L, Momicchioli G, Varriale A. Stability measurements of osseointegrated implants using Osstell in partially edentulous jaws after 1 year of loading: a pilot study. Clin Implant Dent Relat Res. 2002;4(3):128–32.PubMed
45.
Zurück zum Zitat Barewal RM, Oates TW, Meredith N, Cochran DL. Resonance frequency measurement of implant stability in vivo on implants with a sandblasted and acid-etched surface. Int J Oral Maxillofac Implants. 2003;18(5):641–51.PubMed Barewal RM, Oates TW, Meredith N, Cochran DL. Resonance frequency measurement of implant stability in vivo on implants with a sandblasted and acid-etched surface. Int J Oral Maxillofac Implants. 2003;18(5):641–51.PubMed
46.
Zurück zum Zitat Bischof M, Nedir R, Szmukler-Moncler S, Bernard JP, Samson J. Implant stability measurement of delayed and immediately loaded implants during healing. Clin Oral Implants Res. 2004;15(5):529–39.PubMed Bischof M, Nedir R, Szmukler-Moncler S, Bernard JP, Samson J. Implant stability measurement of delayed and immediately loaded implants during healing. Clin Oral Implants Res. 2004;15(5):529–39.PubMed
47.
Zurück zum Zitat Balshi SF, Allen FD, Wolfinger GJ, Balshi TJ. A resonance frequency analysis assessment of maxillary and mandibular immediately loaded implants. Int J Oral Maxillofac Implants. 2005;20(4):584–94.PubMed Balshi SF, Allen FD, Wolfinger GJ, Balshi TJ. A resonance frequency analysis assessment of maxillary and mandibular immediately loaded implants. Int J Oral Maxillofac Implants. 2005;20(4):584–94.PubMed
48.
Zurück zum Zitat Mendonça G, Mendonça DB, Aragão FJ, Cooper LF. Advancing dental implant surface technology–from micron- to nanotopography. Biomaterials. 2008;29(28):3822–35.PubMed Mendonça G, Mendonça DB, Aragão FJ, Cooper LF. Advancing dental implant surface technology–from micron- to nanotopography. Biomaterials. 2008;29(28):3822–35.PubMed
49.
Zurück zum Zitat Miron R, Pikos M. PRF as a Barrier Membrane in Guided Bone Regeneration. Dent Today. 2017;36. Miron R, Pikos M. PRF as a Barrier Membrane in Guided Bone Regeneration. Dent Today. 2017;36.
50.
Zurück zum Zitat Quesada-García MP, Prados-Sánchez E, Olmedo-Gaya MV, Muñoz-Soto E, Vallecillo-Capilla M, Bravo M. Dental implant stability is influenced by implant diameter and localization and by the use of plasma rich in growth factors. J Oral Maxillofac Surg. 2012;70(12):2761–7.PubMed Quesada-García MP, Prados-Sánchez E, Olmedo-Gaya MV, Muñoz-Soto E, Vallecillo-Capilla M, Bravo M. Dental implant stability is influenced by implant diameter and localization and by the use of plasma rich in growth factors. J Oral Maxillofac Surg. 2012;70(12):2761–7.PubMed
51.
Zurück zum Zitat Monov G, Fuerst G, Tepper G, Watzak G, Zechner W, Watzek G. The effect of platelet-rich plasma upon implant stability measured by resonance frequency analysis in the lower anterior mandibles. Clin Oral Implants Res. 2005;16(4):461–5.PubMed Monov G, Fuerst G, Tepper G, Watzak G, Zechner W, Watzek G. The effect of platelet-rich plasma upon implant stability measured by resonance frequency analysis in the lower anterior mandibles. Clin Oral Implants Res. 2005;16(4):461–5.PubMed
52.
Zurück zum Zitat Ergun G, Egilmez F, Cekic-Nagas I, Karaca İR, Bozkaya S. Effect of platelet-rich plasma on the outcome of early loaded dental implants: a 3-year follow-up study. J Oral Implantol. 2013;39(S1):256–63. Ergun G, Egilmez F, Cekic-Nagas I, Karaca İR, Bozkaya S. Effect of platelet-rich plasma on the outcome of early loaded dental implants: a 3-year follow-up study. J Oral Implantol. 2013;39(S1):256–63.
53.
Zurück zum Zitat Kapoor A, Ali AR, Saini N, Gautam K, Goyal A, Prakash V. Comparative evaluation of implant stability with and without autologous platelet-rich fibrin prior to prosthetic loading—a split-mouth randomized clinical trial. J Indian Soc Periodontol. 2022;26(2):137–42.PubMedPubMedCentral Kapoor A, Ali AR, Saini N, Gautam K, Goyal A, Prakash V. Comparative evaluation of implant stability with and without autologous platelet-rich fibrin prior to prosthetic loading—a split-mouth randomized clinical trial. J Indian Soc Periodontol. 2022;26(2):137–42.PubMedPubMedCentral
54.
Zurück zum Zitat Diana C, Mohanty S, Chaudhary Z, Kumari S, Dabas J, Bodh R. Does platelet-rich fibrin have a role in osseointegration of immediate implants? A randomized, single-blind, controlled clinical trial. Int J Oral Maxillofac Surg. 2018;47(9):1178–88.PubMed Diana C, Mohanty S, Chaudhary Z, Kumari S, Dabas J, Bodh R. Does platelet-rich fibrin have a role in osseointegration of immediate implants? A randomized, single-blind, controlled clinical trial. Int J Oral Maxillofac Surg. 2018;47(9):1178–88.PubMed
55.
Zurück zum Zitat Fujioka-Kobayashi M, Miron RJ, Moraschini V, Zhang Y, Gruber R, Wang HL. Efficacy of platelet-rich fibrin on bone formation, part 2: guided bone regeneration, sinus elevation and implant therapy. Int J Oral Implantol (Berl). 2021;14(3):285–302.PubMed Fujioka-Kobayashi M, Miron RJ, Moraschini V, Zhang Y, Gruber R, Wang HL. Efficacy of platelet-rich fibrin on bone formation, part 2: guided bone regeneration, sinus elevation and implant therapy. Int J Oral Implantol (Berl). 2021;14(3):285–302.PubMed
56.
Zurück zum Zitat Neiva RF, Gil LF, Tovar N, Janal MN, Marao HF, Bonfante EA, et al. The synergistic effect of leukocyte platelet-rich fibrin and micrometer/nanometer surface texturing on bone healing around immediately placed implants: an experimental study in dogs. Biomed Res Int. 2016;2016:9507342.PubMedPubMedCentral Neiva RF, Gil LF, Tovar N, Janal MN, Marao HF, Bonfante EA, et al. The synergistic effect of leukocyte platelet-rich fibrin and micrometer/nanometer surface texturing on bone healing around immediately placed implants: an experimental study in dogs. Biomed Res Int. 2016;2016:9507342.PubMedPubMedCentral
57.
Zurück zum Zitat Wang RE, Lang NP. Ridge preservation after tooth extraction. Clin Oral Implants Res. 2012;23(Suppl 6):147–56.PubMed Wang RE, Lang NP. Ridge preservation after tooth extraction. Clin Oral Implants Res. 2012;23(Suppl 6):147–56.PubMed
58.
Zurück zum Zitat Del Corso M, Mazor Z, Rutkowski JL, Dohan Ehrenfest DM. The use of leukocyte- and platelet-rich fibrin during immediate postextractive implantation and loading for the esthetic replacement of a fractured maxillary central incisor. J Oral Implantol. 2012;38(2):181–7.PubMed Del Corso M, Mazor Z, Rutkowski JL, Dohan Ehrenfest DM. The use of leukocyte- and platelet-rich fibrin during immediate postextractive implantation and loading for the esthetic replacement of a fractured maxillary central incisor. J Oral Implantol. 2012;38(2):181–7.PubMed
59.
Zurück zum Zitat BenalcázarJalkh EB, Tovar N, Arbex L, Kurgansky G, Torroni A, Gil LF, et al. Effect of leukocyte-platelet-rich fibrin in bone healing around dental implants placed in conventional and wide osteotomy sites: a pre-clinical study. J Biomed Mater Res B Appl Biomater. 2022;110(12):2705–13. BenalcázarJalkh EB, Tovar N, Arbex L, Kurgansky G, Torroni A, Gil LF, et al. Effect of leukocyte-platelet-rich fibrin in bone healing around dental implants placed in conventional and wide osteotomy sites: a pre-clinical study. J Biomed Mater Res B Appl Biomater. 2022;110(12):2705–13.
60.
Zurück zum Zitat ÖzveriKoyuncu B, İçpınarÇelik K, ÖzdenYüce M, Günbay T, Çömlekoğlu ME. The role of concentrated growth factor on implant stability: a preliminary study. J Stomatol Oral Maxillofac Surg. 2020;121(4):363–7. ÖzveriKoyuncu B, İçpınarÇelik K, ÖzdenYüce M, Günbay T, Çömlekoğlu ME. The role of concentrated growth factor on implant stability: a preliminary study. J Stomatol Oral Maxillofac Surg. 2020;121(4):363–7.
61.
Zurück zum Zitat Gaur S, Chugh A, Chaudhry K, Bajpayee A, Jain G, Chugh VK, et al. Efficacy and safety of concentrated growth factors and platelet- rich fibrin on stability and bone regeneration in patients with immediate dental implants: a randomized controlled trial. Int J Oral Maxillofac Implants. 2022;37(4):784–92.PubMed Gaur S, Chugh A, Chaudhry K, Bajpayee A, Jain G, Chugh VK, et al. Efficacy and safety of concentrated growth factors and platelet- rich fibrin on stability and bone regeneration in patients with immediate dental implants: a randomized controlled trial. Int J Oral Maxillofac Implants. 2022;37(4):784–92.PubMed
62.
Zurück zum Zitat Martino MM, Briquez PS, Ranga A, Lutolf MP, Hubbell JA. Heparin-binding domain of fibrin(ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix. Proc Natl Acad Sci U S A. 2013;110(12):4563–8.PubMedPubMedCentral Martino MM, Briquez PS, Ranga A, Lutolf MP, Hubbell JA. Heparin-binding domain of fibrin(ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix. Proc Natl Acad Sci U S A. 2013;110(12):4563–8.PubMedPubMedCentral
63.
Zurück zum Zitat Serafini G, Lopreiato M, Lollobrigida M, Lamazza L, Mazzucchi G, Fortunato L, et al. Platelet rich fibrin (PRF) and its related products: biomolecular characterization of the liquid fibrinogen. J Clin Med. 2020;9(4):1099.PubMedPubMedCentral Serafini G, Lopreiato M, Lollobrigida M, Lamazza L, Mazzucchi G, Fortunato L, et al. Platelet rich fibrin (PRF) and its related products: biomolecular characterization of the liquid fibrinogen. J Clin Med. 2020;9(4):1099.PubMedPubMedCentral
64.
Zurück zum Zitat Qu C, Luo F, Hong G, Wan Q. Effects of platelet concentrates on implant stability and marginal bone loss: a systematic review and meta-analysis. BMC Oral Health. 2021;21(1):579.PubMedPubMedCentral Qu C, Luo F, Hong G, Wan Q. Effects of platelet concentrates on implant stability and marginal bone loss: a systematic review and meta-analysis. BMC Oral Health. 2021;21(1):579.PubMedPubMedCentral
Metadaten
Titel
The effect of leukocyte- and platelet-rich fibrin on the bone loss and primary stability of implants placed in posterior maxilla: a randomized clinical trial
verfasst von
Meshkat Naeimi Darestani
Hoori Asl Roosta
Seyed Ali Mosaddad
Siamak Yaghoubee
Publikationsdatum
01.12.2023
Verlag
Springer Berlin Heidelberg
Erschienen in
International Journal of Implant Dentistry / Ausgabe 1/2023
Elektronische ISSN: 2198-4034
DOI
https://doi.org/10.1186/s40729-023-00487-x

Weitere Artikel der Ausgabe 1/2023

International Journal of Implant Dentistry 1/2023 Zur Ausgabe

Neu im Fachgebiet Zahnmedizin

Sechs Monate E-Rezept – Erfolgsgeschichte mit Schattenseiten

IT für Ärzte Nachrichten

244 Millionen E-Rezepte sind in sechs Monaten eingelöst worden: Nach einem halben Jahr zieht die Betriebsgesellschaft gematik eine positive Zwischenbilanz. Doch noch sind nicht alle Akteure begeistert.

So können sich Praxen vor Cyberkriminalität schützen

IT für Ärzte Nachrichten

Immer wieder werden Arztpraxen Opfer von Netzverbrechern. Der typische Hacker war einmal, Cyberkriminalität ist sehr vielfältig, berichtet Lars Korunalp. Der IT-Berater gibt Tipps und nennt konkrete Maßnahmen, wie sich Praxen vor Zugriffen aus dem Internet schützen können.

Thüringer Landtag beschließt Vorab-Quote im Medizinstudium

Bewerber, die sich zu einer langen Tätigkeit als Haus- oder Zahnarzt in Thüringen verpflichten, bekommen in Jena künftig leichter einen Studienplatz. Sechs Prozent der Plätze sollen so vergeben werden.

Notfallreform: Lauterbach nimmt KVen und ausgewählte Kliniken in die Pflicht

06.06.2024 Klinik aktuell Nachrichten

Die Ampelkoalition nimmt einen neuen Anlauf für die Reform der Notfallversorgung. Der Gesetzentwurf zeigt: Die Vertragsärzte müssen sich auf erhebliche Veränderungen in der Organisation der Notdienste einstellen.

Update Zahnmedizin

Bestellen Sie unseren kostenlosen Newsletter und bleiben Sie gut informiert – ganz bequem per eMail.