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| ORIGINAL ARTICLE |
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| Year : 2011 | Volume
: 1
| Issue : 2 | Page : 42-50 |
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Five years of clinical and radiographical evaluation of implant survival and dimensional stability of maxillary sinus augmentation procedures performed with platelet-rich plasma
Carlo Maiorana1, Paolo Brivio1, Mario Beretta1, Giovanni Battista Grossi1, Marco Cicciù2
1 Department of Oral Surgery and Implantology, School of Dentistry, University of Milan, Milan, Italy
2 Department of Odontostomatology, University of Messina, Messina, Italy
| Date of Web Publication | 30-Dec-2011 |
Correspondence Address:
Marco Cicciù
Department of Odontostomatoly, School of Dentistry, Messina University, Via Consolare Valeria 98100, Messina
Italy
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/0974-6781.91279
 Abstract | | |
Purpose: Aim of the present study was to present the results of a retrospective analysis of maxillary sinus augmentation procedures performed with platelet-rich plasma (PRP) with a mean follow-up of about 5 years. The analysis was focused on implant survival rates and on the dimensional stability of the subantral cavity filling.
Materials and Methods: Between 2000 and 2006, 28 patients were recruited for a maxillary sinus augmentation procedure performed with PRP. Two patients did not answer to the calling for the examination at distance, so they were excluded from the sample. The study involved 26 patients, for a total amount of 33 sinus augmentations, with an average follow-up of 65 months. In 26 procedures the grafting material used was a mixture of autologous bone taken from the oral cavity, deproteinized bovine bone Bio-Oss® in a relationship of 1:3 and PRP, while in seven cases, the combination of Bio-Oss and PRP. The dimensional stability of grafting material was investigated through X-ray measurements carried out during X-ray postexaminations.
Results: After a mean follow-up time of about 5 years, the implant survival rate registered was 95.9%, while the radiographical variables used to assess the dimensional stability of grafts, showed a mean decrease respectively of 9.38% and 14.61%.
Discussion: Very good long-term results were achieved using autologous bone+Bio-Oss+PRP and Bio-Oss+PRP as filling materials in the maxillary sinus augmentation. Dimensional stability of cavity filling seems to represent a very important factor for implant procedures success. It is difficult to estimate the influence of PRP on a long-term basis.
Conclusion: The implant survival rate obtained in this study was similar to the expected rate on the areas not subject to bone graft. The method applied showed to be reliable for bone regeneration in subantral cavities, showing a very good dimensional stability and a slight reabsorption over the years. Keywords: Dental implants, platelet-rich plasma, sinus lift
How to cite this article:
Maiorana C, Brivio P, Beretta M, Grossi GB, Cicciù M. Five years of clinical and radiographical evaluation of implant survival and dimensional stability of maxillary sinus augmentation procedures performed with platelet-rich plasma. J Dent Implant 2011;1:42-50 |
How to cite this URL:
Maiorana C, Brivio P, Beretta M, Grossi GB, Cicciù M. Five years of clinical and radiographical evaluation of implant survival and dimensional stability of maxillary sinus augmentation procedures performed with platelet-rich plasma. J Dent Implant [serial online] 2011 [cited 2023 Jun 8];1:42-50. Available from: https://www.jdionline.org/text.asp?2011/1/2/42/91279 |
| Introduction | |  |
The treatment of maxillary edentulous jaws with osteointegrated implants is often complex for the frequent coronally pneumatization of the maxillary sinus and for the remaining low bone density. The bone resorption, consequent to the loss of the dental elements, determines atrophy in height, and in thickness, by reducing the amount of available bone to the implant placement. In the 1970s Tatum [1] and then Boyne and James, [2] developed the surgical technique of the maxillary sinus augmentation. The proposed approach represents the most reliable procedure for the bone reconstruction at the maxillary sinus. Many different filling subantral materials have been used over the years. Autologous bone represented for years, the gold standard in bone grafting procedures for his osteoinductive, osteogenic and osteoconductive abilities. On the other hand, the morbidity deriving from the need of a double surgical site has prompted the researchers to develop alternative procedures using alloplastic, eterologous materials and growth factors to support the bone regeneration. [3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14]
Platelet-rich plasma (PRP) constitutes an autologous source of growth factors involved in the osteogenic and angiogenetic procedures. [15],[16],[17],[18],[19] Its use in sinus augmentation has been often supported even if today's debate about its effective usefulness is still open in the scientific community. [20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37]
The aim of this article was to show, through a retrospective analysis of the cases carried out in our structure, the results of using PRP as filling comaterial in maxillary sinus augmentation procedures, in association with heterologous material, with particular focus on the implant survival and the dimensional stability of bone grafts in the course of time.
| Materials and Methods | | |
Patients
Between 2000 and 2006, in the "Implantology Department", 28 patients were subjected to maxillary sinus augmentation procedure, adding PRP on the subantral cavity filling. Among them, two patients were excluded from the sample as they did not attend the medical check-up after at distance.
The study involved 26 patients (18 female and 8 male) with a mean age of 54 ± 9.1 years in between a range of 37-70-years old. One patient was completely edentulous, and the other 25 were partially edentulous in the posterior maxilla [Table 1].
Thirty-three maxillary sinus augmentation procedures were totally performed; one with a one-stage approach and 32 with a two-stage approach plus implant filling 6 months after the grafting procedure.
PRP preparation
According to the PRP preparation protocol, each patient was subjected to the drawing of a whole blood unit (450 cm 3 ) the day before the surgical procedure. The whole unit underwent to two consecutive centrifugations in a gradient of density cells separator. The first centrifugation was performed at 2500 rpm for 8 minutes with a 281-mm centrifugal ray, permitting the separation of blood into its three main components: Red blood cells, PRP and platelet-poor plasma (PPP).
PRP, immediately separated from the other plasmatic components, was subject to a second centrifugation at 3950 rpm for 7.5 minutes with a 281-mm centrifugal ray, permitting a further concentration of platelets in a lower quantity of plasma.
The bag, containing a PRP quantity ranging from 30 to 40 cm 3 , was kept in continuous motion 20°C, until the time of surgery, in order to prevent premature platelet aggregation.
At surgery time, according to the procedure, PRP was transformed in a manageable gel, by platelet aggregation obtained by adding 1 cm 3 of a calcium chloride solution (10%) and two vials of batroxobin (Botropase® Ravizza Farmaceutici Spa Muggiò) as a coagulant factor.
Surgical procedure
For the sinus augmentation, Tatum's surgical lateral procedure was used. Briefly, once a midcrestal incision was made to allow for the lifting of a superior buccal full thickness flap, exposing the atrophic alveolar ridge, an osteotomy, delimiting the bone window, was performed to allow for access to the sinus cavity, the mobilization of the Schneiderian membrane, creating a virtual cavity fit, to receive the grafting material. During the surgical procedure the PRP was transformed in a manageable gel according to the described process.
For 26 sinus augmentation procedures the grafting material was composed of a mixture of autologous bone taken from tuber and neighbouring areas by the use of Safescraper (Meta, Reggio Emilia, Italy), and deproteinized bovine bone bio-OSS® (Geistlich, Wolhsen, Switzerland), in a relationship of 1:3 and PRP; for the other seven procedures, only the combination of bio-OSS and PRP has been used.
During the study, 28 Branemark implants were inserted (Nobel Biocare, Goteborg, Sweden), 25 Frialit-2® implants (Friatec AB, Mannheim, Germany), 7 Camlog implants (Altatech), 5 T.B.R. implants (Benax, Ancona, Italy), 4 3i® implants (Implant Innovations, Inc. USA) e 2 Astra implants (Astratech, Goteborg, Sweden) for a total amount of 73 implants inserted in grafted sites.
Six months after the grafting procedure implants were inserted. Twenty-five patients received a fixed prosthetic rehabilitation and 1 patient a removable prosthesis with a bar anchored to the implants [Table 2]. | Table 2: Number of sinus augmentations and implants according to the grafting material
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Rx findings
For the radiographical evaluations, panoramic X-rays were taken immediately after augmentation and after an average period of observation of 65.23, 97 months, with a minimum of 31 and up to 100 months.
X-rays were carried out all with the same machine and the same radiographical film: Siemens Orthophos (Germany) e Kodak Dental film.
X-rays poorly observable or affected by head positioning errors were not taken into consideration for the measurements of the changes of grafting material during time.
X-rays taken into consideration were scanned and became digital printings to be evaluated with a digital program. In order to obtain correct measurements, software Acrobat Reader Professional 7.0 were used. This software, on the basis of well-known measurements such as the length of the implants in the panoramic images, led to obtain a scale to compare measurements studied.
Thirty-six X-rays as a total have been taken into consideration on 18 patients. According to Hatano et al., [38] four variables were measured and recorded by the measurement instrument of the software. In order to evaluate changes in each implant's sinus-graft, following variables were considered:
- Implant length (IL) defined as the distance between the apex and the head of the fixture
- Bone Level (BL) defined as the distance between the highest level of the grafted sinus floor on each implant and the implant's head itself.
In order to evaluate changes in sinus-graft height compared to the original sinus floor following variables were considered: - Original Sinus Height (OSH), defined as the distance between the bone intraoral margin and the lowest point of the original sinus floor
- Grafted Sinus Height (GSH), defined as the distance between the bone intraoral margin and the new grafted sinus floor located over the lower point of the original sinus floor (OSH) [Figure 1].
 | Figure 1: IL - Implant length; BL - Bone length; OSH - Original sinus height; GSH - Grafted sinus height
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In order to state the relationship between the sinus graft height and each implant, the BL ratio as BL/IL was introduced. A value exceeding 1 indicates that the grafted sinus floor is above the implant apex; a value less than 1 means that the grafted sinus floor is below the implant apex and the implant apex is not completely covered by the sinus floor.
Similarly, GSH/OSH ratio was introduced the. A value exceeding 1 indicates that the grafted sinus floor is above the original sinus floor. This ratio has been used to compare the sinus graft height on the not-implants-supported areas.
Implants were divided into three groups based on the height of the grafted sinus floor relative to the implant apex:
- Group I, in which the grafted sinus floor was above the implant apex;
- Group II, in which the implant apex was level with the grafted sinus floor; and
- Group III, in which the grafted sinus floor was below the implant apex
| Results | | |
Implant survival rate
At the time of the first check-up, corresponding to the implant uncover, 3 of 73 implants were classified as not integrated, thus removed and showing a premature failure rate of 4,1%. Particularly, two implants were lost after being lifted with Bio-Oss and PRP, one with mixture of autologous Bio-Oss and PRP. After those failures, during the whole observation period, (65.18 ± 23.97 months minimum 31, up to 100 months), no failures were recorded, bringing to a cumulative survival rate of 95.9%. Following Tables show in detail the cumulative survival rate in relation to the observing period and to the graft type [Table 3] and [Table 4].
Radiographic evaluation of graft height changes
In order to perform a clinical long-term evaluation of the dimensional stability of the sinus grafts, 36 panoramic X-ray images, of 18 patients and showing 256 measurements, were used. The average value of the ratio BL/IL, immediately measured after the placements of implants, was 1.30 ± 0.25. The same ratio, after an average observation period of 65.18 ± 23.97 months, was 1.17 ± 0.21 with an average decrease of 10%. The average ratio value exceeding 1 indicates that the implant apex remains covered by the grafted sinus floor, even after many months, for most of the implants [Table 5].
The average value of the ratio GSH/OSH decreased of 15%, from 3.31 ± 1.55 at first measurement, to 2.81 ± 1.14 at the time of the control. The average value of the ratio exceeding 1, indicates that the grafted sinus floor is above the original floor, even after 5 years [Figure 2], [Figure 3], [Figure 4] and [Figure 5]. | Figure 2: BL changes between first and second measuring in mm (a) and in percentage (b)
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 | Figure 3: GSH changes between first and second measuring in mm (a) and in percentage (b)
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 | Figure 4: BL changes in mm (a) and in percentage; (b) according to Autologous+Bio-Oss+PRP group
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 | Figure 5: GSH changes in mm (a) and in percentage; (b) according to Autologous+Bio-Oss+PRP group
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Taking into consideration BL and GSH values, at the time of the clinical exam, they decreased respectively of 9.38 ± 0.08% and 14.61 ± 0.10%.
Following graphics show the changes of measurements on the OPTs, in general and related to the specific implant [Figure 6], [Figure 7] and [Figure 8]. | Figure 6: BL changes in mm (a) and in percentage; (b) according to Bio-Oss+PRP group
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 | Figure 7: GSH changes in mm (a) and in percentage; (b) according to Bio-Oss+PRP group
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 | Figure 8: Mean BL and GSH changes according to Autologous+Bio-Oss+PRP group and to Bio-Oss+PRP group
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| Discussion | | |
The objectives of this retrospective analysis, performed on the clinical experience of "Implantology Department", were the evaluation of implant survival and dimensional changes of subantral grafting material during time.
Data were obtained from archives analyses and both radiographical and clinical exams of the patients, during the period 2000 and 2008.
In literature, many different clinical implant survival rates have been reported, varying between 70 and 100%. Results' variation depends on different factors: Different follow-up, inclusion criteria, used materials, prosthetic and surgical treatments. All those factors complicate the comparison of different studies.
The implant-prosthetic rehabilitating treatment of the sample, led to obtain a implant survival rate of 95.9%, with an average examination period of 5 years. This survival rate is very similar to the recently evaluated cases in a retrospective investigation on 10 years of clinical activity of Implantology Department. Bone regeneration stability and the reliability on the maintenance of the osteointegration after many years are confirmed by the absence of implants failures after a period of time.
The different implant survival rate between the autologous+Bio-Oss+PRP group and the Bio-Oss+PRP group can not be considered statistically valid because of the not homogeneous number of patients included in the two groups.
Dimensional stability of cavity filling represents a very important factor for success of implant procedures. Many different clinical and observational studies showed that using different materials, such as autologous bone, deproteinized bovine bone and others, could be clinically effective and predictable. [39],[40],[41],[42],[43],[44],[45],[46]
Autologous bone has been considered the gold standard for years, but its use could be limited by the donator's morbidity, by its reduced availability and by its variable resorption.
Different authors proposed the use of eterologous materials such as deproteinized bovine bone, which low resorbing characteristic could maintain the implant's volume during the years. [47],[48],[49]
The data, collected by panoramic image's measurements, showed an average reduction of the graft height of 9.38 ± 0.08% in the areas supporting implants and of 14.61 ± 0.10% in the interimplant areas. This difference may suggest a stabilizing effect the graft height maintenance by the loads applied to implants. Similarly, the preservation of graft height and so its dimensional stability may be associated with an absence of implant failures after a period of time.
In the sample, a good relation between the graft and the implant during the years was confirmed by measurements taken for each implant inserted in the reconstructed bone.
As a conclusion of this retrospective analysis, it is possible to sustain that very good long-term results were achieved both using the mixture of autologous bone+Bio-Oss+PRP and of Bio-Oss+PRP, as grafting materials in the sinus augmentation procedures. Dimensional stability of cavity filling seems to represent a very important factor for implant success.
It is difficult to measure the influence of PRP over the long-term results. The rational principle which constitutes the basis of using PRP as a stimulus for bone regeneration consists in the possibility of concentrating the growth factors included in platelets and addressing them in regenerating sites through an ideal carrier, which are the patient's platelets.
During the bone regeneration process, the growth factors play an important role both at the beginning and in maintaining the differentiation and proliferation of osteoprogenetic cells and osteoblasts, which lead to the regeneration of the new bone.
In the early phases, TGF-b and PDGF released by platelets admitted to form the clot, promote the maturation of the osteoprogenitor cells towards the osteoblastic line in combination with the growth factors released by the traumatized bone tissue.
The whole combination of these tissue-repairing promotion activities stimulates specifically the expression and the synthesis of other regulating factors of macrophages and osteoblasts occurred in the regenerating site. [50] Among them BMPs synthesized by endosteal osteoblasts, early emerge thus contributing to the osteoblastic differentiation of totipotency mesenchymal cells.
Once the regenerating process has started, it can automatically maintain a high proliferative and metabolic level, through the synthesis of the same growth factors by osteoblasts implicated in the process, also sustained by capillary angiogenesis promoted by the PDGF. [51],[52],[53]
Because of its nature, the effect of PRP blows over in the first 2 weeks after the grafting procedure; while in the long period the osteoconductive characteristics of the graft prevail. It is possible that the fibrin texture resulting from the polymerization of fibrinogen contained in the PRP clot provides to the bio-OSS graft a further framework or "binary guide" for the migration of osteoblasts in contact with the surface of the granules of bio-material, and that growth factors platelet enhance the potential regeneration, even in a little active grafting site like the subantral cavity of the maxillary sinus.
According to the literature, many different benefits have been proposed to use PRP for sinus augmentation:
- Higher quantity and quality of the regenerated bone; [15],[17],[54],[55]
- Reduction of the osteointegration time; [56]
- Improvement of the healing of soft tissues; [23]
- No risk of illness transmission; [57]
On the other hand there have been raised limitations on its use:
- Need of vital cells to became a bone regeneration stimulus; [17]
- Limited time effect; [58],[59]
- Low number of platelets determines limited time effects; [17]
- Different ways of preparation could invalidate platelets' physiology modifying the ability of producing growth factors;
A recent literature review [60],[61] showed how since 2000 many different studies upon animals and humans have been published regarding PRP as a filling material in sinus augmentation, but many of them are incomplete from a scientific point of view and they often bring to positive solutions without being supported by a right design of the study itself.
In conclusion, only a few scientifically proven data exist on the benefit of adding PRP to the usual procedures of sinus augmentation.
Theoretically, PRP has many positive effects, such as being an autologous source of growth factors, which is able to cure wounds by itself, nevertheless its use cannot be supported on the basis of the literature and other randomized and controlled studies have to be performed before giving a unique opinion on its routine use.
| Conclusions | | |
Clinical survival rate of implant obtained in this retrospective study confirms the validity of the subantral filling procedure. The use of eterologous bone as substitutes led to bone regeneration, reliable from an implant survival and dimensional stability point of view, showing a very low radiographical resorption. We cannot provide a final evaluation judgment on the PRP filling long-term results, other prospectical studies have to be performed in order to evaluate PRP routine-use in sinus augmentation for pre-implant purposes.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]
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