Efficacy of platelet-rich fibrin in maxillary sinus augmentation and simultaneous implant placement in deficient maxillary ridges: A pilot comparative study

Abstract

Background

Rehabilitation with dental implants has become the most widely accepted treatment protocol for rehabilitation of lost natural teeth. Direct sinus lift is one of the most predictable procedures for augmenting the deficient posterior maxillary ridges.

Methods

The study was designed in patients with insufficient bone for implants in the maxillary posterior ridges. The test group received platelet-rich fibrin alone as filler, and the control group received a bone allograft. The residual bone height (RBH), implant mobility, and soft tissue characteristics between and within the groups were compared and analyzed.

Results

Both the groups had considerable gain in RBH, and the intragroup analysis revealed clinical gain in bone height in both the groups, with the test group exhibiting statistically significant gain which kept on improving from 6 months with z= -3.477 and a p value of 0.001 to 9 months with z=-3.531 and a p value of 0.027.

Conclusion

The results suggest that the use of platelet-rich fibrin alone improves the bone regeneration, thereby achieving predictable and stable augmentation of the sinus floor required for the success of implant therapy.

Introduction

Dentistry and the associated clinical specialities are under constant challenge to widen the knowledge base and to foster newer skills and methods to meet the ever-growing requirement of the present generation. High expectations in terms of esthetics and functionality have triggered exponential growth in biologic and material sciences, which in turn bring the best out of the practising clinician.

Implant-supported dentures are categorized one of the breakthrough inventions of the century in clinical dentistry. The untiring work of Dr Branemark has led to the development of the concept of osseointegration and dental implants in the latter half of the twentieth century.¹ Since then, Implantology has developed in a neck break speed with the development of new implant systems, improved diagnostic procedures and introduction of novel surgical techniques.

Sinus lift or sinus augmentation is considered one of the most predictable procedures for augmenting the deficient or defective bone in the maxillary molar and premolar regions. The current techniques using lateral as well as axial approaches have proven to be successful to provide a sufficient quantity of bone for the placement of endosteal dental implants.2, 3, 4 A success rate of 95–96% has been reported when the procedure is performed as a pre-prosthetic surgery,^5,6 and this success is often attributed to the highly osteogenic potential of the Schneiderian membrane, which may increase the efficiency of most of the materials used for augmentation.⁷ Studies have shown that sinus lift can be performed using the lateral approach with whole blood as the sole filling material provided the blood clot is stabilized in the sinus cavity.⁸

The platelet-rich fibrin (PRF) was first described by Dohan et al, in 2001.⁹ PRF prepared from centrifuged blood is a second-generation platelet concentrate.¹⁰ It contains various growth factors at a higher amount, which are involved in key stages of wound healing and regenerative processes including chemotaxis, proliferation, differentiation, and angiogenesis.

The aim of the study was to compare the efficacy of PRF alone with that of a bone allograft for augmentation of sinus floor using a lateral window approach for immediate placement implants in cases with deficient maxillary ridges. The objectives were 1) to compare the efficacy of PRF, used as the filler and the membrane, with that of a bone allograft (DFDBA) and collagen membrane for bone augmentation in maxillary sinus lift procedures, 2) to assess the peri implant tissue characteristics, and 3) to evaluate radiographically the residual bone height (RBH) between the maxillary sinus and the implant postoperatively after 6 months.

This in vivo pilot study was undertaken to augment the maxillary sinus so as to place endosseous implants and thereby provide the patients with implant-supported dentures. PRF alone was used as the graft material and the membrane in the test group and DFDBA and collagen membrane was used in the control group. The gain in RBH, thus, achieved along with the peri implant tissue characteristics required for successful implant treatment were compared and analyzed.

Material and methods

This in vivo, clinical study was conducted in a tertiary care teaching institution after obtaining the approval from the Institutional Ethical Committee (IEC) and scientific/medical research committee (MRC).

Sample size calculation

The sample size estimation was done according to the specified sampling frame wherein a 10% increase in sample size was taken so as to adjust for cases lost to follow-up. A parallel study design was formulated with two study groups of 15 patients in each group (Group A&B). To overcome the inter-individual variability and to ensure accurate results with a lower risk of bias, randomization was done by a simple random sampling method and also matching both the groups for age and gender.

The following were taken into consideration in the study:

Inclusion criteria

• a)Patients of either sex within the age group of 20–60 years with partial edentulousness in the posterior maxillary arch.
• b)Clinical and radiological diagnosis of insufficient height of maxillary bone for the placement of single or multiple implants (RBH 4–6 mm).
• c)Clinical and radiological diagnosis of large sized maxillary sinus.
• d)Absence of acute or chronic maxillary sinus inflammation.
• e)Patients with acceptable oral hygiene.

Exclusion criteria

• a)Patients with the presence of systemic conditions or disease affecting bone density, for example, osteoporosis and Paget's disease.
• b)Patients with aggressive periodontitis.
• c)Patients with uncontrolled diabetes mellitus, ongoing chemotherapy or radiotherapy or other contraindicating systemic conditions.
• d)Patients with a history of drug intake that can affect bone metabolism in the past 6 months. For example, NSAIDs, bisphosphonates, etc.
• e)Patients who are current smokers or ex-smokers for less than 5 years.
• f)Pregnant or lactating females.
• g)Patients with alcohol dependence syndrome.
• h)Immunocompromised patients.
• j)Patients with gross oral/maxillary sinus pathology and tumors.

Fourty patients attending the central OPD of the department were selected and assessed for eligibility in the study. A total number of 30 systemically healthy subjects with deficient posterior maxillary ridges and meeting all the other inclusion and exclusion criteria were finally included in the study. The selected patients were aged between 26 and 47 years.

The selection and randomization into different groups were done following the guidelines and instructions as per the Helsinki declarations and good clinical practices guidelines (GPC). All the patients were informed about the treatment plan and the surgical procedure in their own vernacular language and written informed consents were obtained in both English and the regional language.

The selected patients underwent all the routine preoperative, clinical, laboratory, and radiological assessments. Clinical evaluation and history were repeated in each case to rule out any recent respiratory conditions or sinusitis and related conditions. Digital orthopantomograms (OPGs) and intraoral periapical radiographs of the involved teeth were taken to study the maxillary sinus location and outline as well as to measure the RBH. Study models were prepared to evaluate the ridge characteristics in terms of height, width, and inter occlusal distance. Pre-operatively only the baseline parameter of RBH was recorded.

The design of the study required the patients with posterior maxillary ridge defects to be randomly divided into two groups:

Group A: The test group received only PRF as the filling material in the sinus cavity and the prepared PRF membrane to cover the buccal window following a lateral sinus lift procedure and placement of implant with platform switch design immediately.

Group B: The control group received DFDBA as the filling material and a collagen membrane was used to cover the buccal window prepared for sinus augmentation.

The included parameters:

• 1.Residual bone height in mm

The RBH was determined and recorded to the nearest 0.5 mm on the OPG without magnification preoperatively and after 6 months and 9 months of sinus augmentation with the same OPG (Planmeca) machine at a fixed coefficient of deformation of x 1.3. The height was measured digitally from the lowest margin of the maxillary sinus to the lowest margin of the alveolar ridge in the dentulous posterior maxilla.

• 2.Periotest value for mobility

The mobility of the implants was tested using Periotest (Medizintechnik Gulden, Germany) by placing the tip of the equipment on the buccal aspect at the implant-crown junction. The Periotest values are graded from ^-8 to ⁺50, with the values of ^-8 having the highest stability and ⁺50 the highest mobility. The readings were taken first at 6 months post implant placement and then repeated after 3 months.

The other clinical measurements were taken by using a plastic-tipped periodontal probe and the measurement was recorded to the nearest 0.5 mm. This included the probing depth and the probing attachment level (PAL). The modified plaque index (mPI) and the modified bleeding index (mBI) were recorded by the method as described by Mombelli et al, in 1987 around the implants.¹¹

A cooling centrifuge was used to prepare the PRF using the method as described by Choukroun et al. On the day of surgical procedure, 72 ml blood was collected from the antecubital veins of the patients into nine glass-coated vacutainers without any anticoagulant. Immediately after collection, the tubes were then spun in the centrifuge for 12 min at 2700 rpm. The resultant fibrin clot, which is located in the centre of the tube with the red blood cell base is taken out with the help of tissue pliers, and the clot is separated from the red cell base using a sharp scissor. 1–2 clots were gently compressed between two sterile gauze pieces to obtain the PRF membranes and the remaining PRF clots were used to fill the sinus cavity.

Surgical procedure

All the procedures were performed under local anaesthesia using 2% lignocaine hydrochloride with adrenalin 1:80,000 by administering an infraorbital, posterior superior alveolar, and greater palatine nerve block and through a subperiosteal infiltration. A full-thickness muco-periosteal flap was elevated after giving a mid or para crestal incision and two vertical incisions. The outline of the lateral wall window on the buccal plate was demarcated using the round surgical tip of the piezo surgical unit (Fig. 1). The lower border of the window was kept approximately 3 mm above the sinus floor and the upper border was kept depending on the site and length of the implant. The mesial and distal borders were outlined so as to keep the size of the window at about 15–20 mm.² The osteotomy cuts were deepened till the bluish hue of the sinus membrane was visible. The upper border of the cut was kept shallower than the other three margins so that the lateral window stays connected to the buccal plate. This was followed by an in-fracture by applying gentle pressure by a blunt instrument to get the bony access window into the maxillary sinus. The sinus membrane was then detached using specialized direct sinus lift instruments and the peizotome. After detaching the membrane from the floor the sinus was elevated carefully starting from the sinus floor and then toward the mesial and distal walls of the cavity with the help of the direct sinus lift instruments. The sinus membrane integrity was tested by observing the membrane lifting when the patient was deeply breathing in. After elevating the sinus membrane to the desired height depending on the length of the implant to be placed, immediate implant placement was carried out by performing implant osteotomy through the crestal approach (Fig. 2).

Fig. 1.

Test group—surgical preparation.

Fig. 2.

Test group—sinus lifting and implant placement.

In the test group, after the implant placement the sinus cavity was filled with the PRF clots. The sinus membrane after elevation and immediate implant placement was maintained like a tent with the implant tip acting as the tent strut and the PRF clot all around it. The PRF membrane which was prepared earlier was used to cover the buccal window (Fig. 3). Following this the tension free closure of the muco-periosteal flap was achieved with a non-resorbable, 3-0 silk suture material by horizontal mattress sutures or interrupted sutures.

Fig. 3.

Test group—platelet-rich fibrin clot and membrane positioning.

The patients were recalled for review on the first postoperative day and after 4–7 days for review and the sutures were removed, and the surgical area was flushed with sterile saline and povidone iodine solution. During the recovery phase, the patients were recommended to take all the requisite oral hygiene measures.

The patients were recalled after 6 months for exposing the implants and placement of healing caps or gingival formers. Prosthodontic rehabilitation was carried out immediately after recording the necessary study parameters at this point of time, that is, 6 months after sinus augmentation the RBH was recorded (Fig. 4). The patients were again recalled after 3 months (9 months after initial surgery) and all the parameters were obtained, compared and statistically analyzed.

Fig. 4.

Test group—pre- and post orthopantomogram.

In the control group, the technique used was the same except that DFDBA was used for sinus augmentation and a resorbable collagen membrane was used to cover the buccal window (Fig. 5).

Fig. 5.

Control group—surgical procedure with pre- and post orthopantomograms.

Results

The statistical analysis of all the parameters was performed using an SPSS (Statistical Package for Social Sciences) Version 24.0 (IBM Corporation, Chicago, USA). The normality of data was analyzed by the Shapiro–Wilk test. The Mann–Whitney U-test and Wilcoxon signed rank tests were used to check differences between groups wherever appropriate.

The mean RBH value of 5.46 (S.D 0.74) and 5.33 (S.D 0.72) at baseline in test and control groups had increased considerably to 13.40 (S.D 0.98) and 13.20 (S.D 1.20) at 6 months and to 13.53 (S.D 0.23) and 13.20 (S.D 0.34) at 9 months, respectively. The intragroup analysis revealed clinically as well as statistically significant gain in bone height in both the groups with the test group exhibiting a slightly better gain, which improved from 6 months with z = −3.477 and p-value of 0.001–9 months with z = −3.531 and a p-value of <0.001 (Fig. 6) (Table 1).

Fig. 6.

Comparative analysis of residual bone height.

Table 1.

Intragroup comparison of mean residual bone height (in mm) from baseline to 6, 6 to 9, and baseline to 9 months.

Grp	Timeline	N	Mean	S.D.	S.E.	M.D.	95% C.I.	Z-value	P-valuea
PRF	Baseline	15	5.46	0.74	0.19	−7.93	−8.32–7.54	−3.477	0.001b
	6 months	15	13.40	0.98	0.25
	6 months	15	13.40	0.98	0.25	−0.13	−0.41-0.15	−1.000	0.317
	9 months	15	13.53	0.91	0.23
	Baseline	15	5.46	0.74	0.19	−8.06	−8.39–7.73	−3.531	<0.001b
	9 months	15	13.53	0.91	0.23
DFDBA	Baseline	15	5.33	0.72	0.18	−7.86	−8.32–7.40	−3.473	0.001b
	6 months	15	13.20	1.20	0.31
	6 months	15	13.20	1.20	0.31	0.00	−0.29-0.29	0.000	1.000
	9 months	15	13.20	1.32	0.34
	Baseline	15	5.33	0.72	0.18	−7.86	−8.41–7.31	−3.455	0.001b
	9 months	15	13.20	1.32	0.34

^aP-value derived from Wilcoxon signed rank test.

^bsignificant at p < 0.05.

The mean perio test value (PTV) of −3.80 (S.D 1.32) and – 3.06 (S.D 0.79) in test and control groups at baseline reduced to – 3.86 (S.D 0.664) and −2.93 (S.D 0.79) at 9 months, respectively. The difference in the reduction in PTVs between the two groups were statistically significant with z= (−2.215) and a p-value of 0.027 (significant since p-value < 0.01 by Mann–Whitney U-test) (Fig. 7), (Table 2).

Fig. 7.

Comparative analysis of implant mobility.

Table 2.

Intergroup comparison of mean periotest value for implant mobility between the two groups.

Time	Groups	N	Mean	S.D.	S.E.	M.D.	95% C.I.	Z-value	P-valuea
Baseline	Platelet-rich fibrin (PRF)	15	−3.80	1.32	0.34	−0.73	−1.54-0.08	−1.453	0.146
	DFDBA	15	−3.06	0.79	0.20
9 Months	PRF	15	−3.86	1.18	0.30	−0.93	−1.69–0.17	−2.215	0.027b
	DFDBA	15	−2.93	0.79	0.20

^aP-value derived from Mann–Whitney U-test.

^bsignificant at p < 0.05.

The values of probing pocket depth, the PAL and the mPI were not statistically significant. However intergroup comparisons for the modified bleeding index scores revealed significant improvement from the baseline through 9 months with p-values < 0.05 by Mann–Whitney U Test.

Discussion

Edentulousness is one of the commonest problems for which definitive rehabilitation have to be carried out since it affects both function and esthetics.¹² Increasing number of patients are being given implant-supported restorations because of their predictability.¹³ Research in the field have proved clearly that rehabilitation with dental implants have significantly improved the patient's quality of life as they increase the patient's comfort and self-confidence.^14,15

Defective or deficient maxillary ridges with insufficient amount of maxillary bone and approximation of the maxillary sinus to the ridge due to it’s large size and shape are relative contradictions for implant placement since sinus floor augmentation can help in overcoming the situation. Success of the procedure has been reported as high as 97%.^16,17

Maxillary sinus lift can be done by a direct or lateral sinus lift approach and an indirect or crestal approach. The lateral approach is done by a Caldwell-Luc osteotomy where the maxillary sinus floor is grafted to provide a sufficient quantity of bone for the placement of endosteal dental implants while in the direct technique the sinus is accessed through the crestal bone. The Schneiderian membrane is like the periosteum having a very high osteogenic potential. The triad of tissue engineering can be applied by harnessing this potential with a platelet derivative such as PRF and thereby the practitioner can accelerate the sub sinus bone formation and early osseointegration of the implant. Platelet rich fibrin (PRF) prepared from autologous centrifuged blood is a concentration of platelets and leukocytes enmeshed in the fibrin framework and containing various growth factors at a higher amount which are involved in important stages of wound healing and regenerative processes including chemotaxis, proliferation, differentiation and angiogenesis. The main growth factors include platelet derived growth factor, transforming growth factor, fibroblast growth factor, vascular endothelial growth factor and insulin like growth factor.¹⁸ The local delivery of biologically rich growth factors in environment during the osseointegration of dental implant is the most primary reason for achieving better results in Group A in this study.

The use of Ultrasonic bone surgery (USBS) by means of the piezo surgical unit can enhance the success rates of maxillary sinus lift procedure as it selectively cuts through the hard tissue without causing any damage to the adjacent soft tissue.¹⁹ The vibrations of the tip is generated by a piezoelectric transducer, when the tips are activated, the soft tissues namely the gingiva, membranes, vessels and nerves vibrate with the tip and thus is preserved from being damaged.²⁰

In this study, at the end point, in the intragroup comparison at varying timelines, the gain in RBH was clinically as well as statistically significant with p-values < 0.001. It was seen that in the test group the rate of gain in bone height was more compared with that in the control group which is in agreement with earlier studies conducted with PRF for sinus augmentation alone or in combination with other graft materials.^21,22 The mobility, although showed marked improvement clinically, the difference between both the groups were statistically significant at the end of the study with PTV measurements having a less mean value of −3.86 in the test group, −2.93 in the control group and a p-value of 0.027 suggesting more natural bone formation around the implants in the PRF group.

The mBI score is the other value that showed significance. The improvement in the scores may be attributed to the inward movement of the IAJ due to platform switching design of the implant, which causes a thickening of the connective tissue thickens laterally, which increases blood flow around that area and thereby preserving the health of the peri-implant hard and soft tissue.²³

The present study within its limitations, projects the importance of incorporating PRF, which is rich in growth factors into the sinus cavity for achieving a clinically acceptable and predictable outcome.

Conclusion

The present study compared PRF and DFDBA for sinus floor bone augmentation and simultaneous implant placement in deficient maxillary ridges. The PRF group showed consistent increase in the RBH and lesser implant mobility scores. It may be surmised that the concepts of tissue engineering in which the osteogenic potential of the sinus membrane is enhanced by signaling molecules, which are released by the autologous PRF as is evident from this study.

Rehabilitation of deficient posterior maxillary ridges by regeneration and the augmentation of the maxillary sinus floor is a price that the clinicians are willing to pay for with its inherent difficulties. Research is continuous to reach at a point where replacement of the lost tooth structure is possible as less traumatically as possible with the help of the ever expanding scientific knowledge.

Disclosure of competing interest

The authors have none to declare.