Implant therapy for rehabilitation of posterior maxillary regions often presents a challenge because of inadequate quantity and poor bone quality of edentulous alveolar ridge. The maxillary sinus augmentation procedure (SAP), initially published by Boyne and James1 and described by Tatum,2 was introduced to augment ridge volume, by placing graft material between the sinus membrane and the residual alveolar ridge. Since then, the sinus augmentation (SA) procedure has been shown to be a predictable technique to increase available bone height in deficient posterior maxillary ridges before implant placement.3–7 Various approaches have been proposed to achieve the necessary bone volume for the insertion of implants in the atrophic posterior maxilla.3,8
The lateral wall SA approach is considered one of the most predictable preprosthetic surgical techniques. Recent systematic literature reviews have demonstrated that the SA procedure results in a well-documented overall implant survival rate above 90%.3–7 Several graft materials for SA have been used, such as autogenous bone, allografts, xenografts, alloplastic materials, and combinations of these materials.8–13 However, according to the literature, such heterogeneity may not influence clinical outcomes, when rough surface implants are used.6,14,15
More recently, growth factors (GFs) have been used to accelerate the healing process and induce an optimal cellular response. Among the GFs, plasma rich in growth factors (PRGFs) have demonstrated the potential to influence bone regeneration.17 The PRGF has been used in combination with xenografts as grafting material in bony defects.17 However, there are limited studies that report on the use of PRGF in SAs when considering long-term implant survival.18,19
The aims of the present retrospective case series study were to identify determinants of long-term implant survival after maxillary SAPs using a combination of PRGF and graft substitute material, consisted mainly of xenograft.
Materials and Methods
A retrospective case series study design was used. The study included patients treated at private practice in A Coruna, Spain from 2000 to 2014. Data analysis was designed to preserve the anonymity of the patients. Clinical charts of potential patients were carefully reviewed, including computed tomography (CT) scans and panoramic radiographs, to identify patients that conformed to the inclusion criteria. Inclusion criteria included those patients (1) who were over the age of 18, (2) who had undergone a SAP using a lateral wall approach, (3) who were treated using PRGF in combination with xenograft (with or without autogenous graft harvested from lateral wall osteotomy) as the graft material, and (4) whose implants were restored for at least 1 year from the time of implant placement. Consecutive patients that fulfilled the inclusion criteria were selected for this study. There were no exclusion criteria. The STROBE (Strengthening the Reporting of Observational studies in Epidemiology) guidelines20 were followed to write this manuscript. Protected health information with any identifiable information was not included during this study. Written and oral consent was obtained from each patient before treatment. The present study was reviewed and approved by Ethical Committe at A Coruña-Ferrol (Spain) (#2016/394).
In 92 of 100 treated sinuses, anorganic bovine bone mineral (ABBM) (Bio-Oss; Geistlich Pharma, Wolhusen, Switzerland) was used in combination with PRGF (PRGF; BTI Biotechnology Institute, Vitoria, Spain). A combination of ABBM, PRGF, and autogenous bone obtained from either the remaining bone in the lateral wall or implant osteotomy (in one stage implant placement) was used in 8 of the remaining sinuses. A variable amount of total bone graft material, ranging from 3 to 7 mL, was used per sinus.
In all the cases, the harvested PRGF was prepared after manufacturer's instructions (PRGF; BTI Biotechnology Institute, Vitoria, Spain), whose technique protocol was previously described.17,21
Two different types of implants were placed: 164 implants were BTI Externa (BTI; Biotechnology Institute, Vitoria, Spain) and 53 implants were Brånemark Mk IV TiUnite (Nobel Biocare AB, Göteborg, Sweden). Implant diameters ranged from 3.3 to 5.5 mm and from 8.5 to 15 mm in length. All implants (20) placed in sinuses grafted with PRGF + ABBM + autogenous bone were Brånemark Mk IV TiUnite.
Patients were treated in the same dental office and by the same clinician (Dr. José Pardiñas Arias). All surgeries were planned using CT scans (Fig. 1). All patients were premedicated with antibiotic prophylaxis (amoxicillin 2000 mg or clindamycin 600 mg) depending on the history of drug allergy 1 hour before the SAP. The modified Caldwell-Luc surgical procedure, as described previously,12 was performed to gain access to the sinus cavity.
Local anesthesia (Lidocaine HCl 2% with 1:100,000 epinephrine, Lidocaine HCl 2% with 1:50,000 epinephrine, mepivacaine/Carbocaine 3% without epinephrine, or Bupivacaine HCl 0.5% with 1:200,000 epinephrine) was administered in the buccal and palatal regions of the surgical area. A midcrestal incision was made, and a full thickness mucoperiosteal flap was reflected. Vertical releasing incisions extending past the mucogingival junction were made when necessary.
The antrostomy was then performed in the lateral wall of the maxillary sinus by means of a piezoelectric unit (Piezosurgery; Mectron, Carasco, Italy) under copious sterile saline irrigation to access the sinus (Fig. 2A). The size of the window was made according to the size of the implant that was to be placed by measuring from the crest to the length of the implant along the lateral sinus wall. The window of the lateral sinus wall was preserved or removed to be used in combination with the bone substitute. The sinus membranes were elevated using the piezoelectric unit and hand instruments. Care was taken not to perforate the sinus membrane.
Thirty milliliters of the patient's blood was taken by venipuncture before surgery and placed directly into 5 mL tubes which contained 3.8% (wt/vol) sodium citrate as anticoagulant. The PRGF was prepared by centrifugation at 460g for 8 minutes at room temperature. The 0.5 mL plasma fraction located just above the red cell fraction and white cell fraction was collected from each tube and deposited in a glass dish. After adding 0.5 μL of calcium chloride per milliliter of plasma, activation and clotting were initiated. The combination of ABBM and PRGF allowed for the formation of a clot incorporating the bovine bone (Fig. 2B). The latter facilitated the manipulation and placement of the graft (Fig. 2C). In cases in which the sinus membrane was perforated, the membrane was repaired using a layer of active PRGF.
The decision to place implants simultaneously or after a delay was made by the operator depending on residual crestal bone height (RBH), bone quality, and if primary implant stability could be achieved using a minimum of 15 N/cm of torque. After this, the remaining of the surgical procedure was dependent on whether or not implants were placed.
Simultaneously or One Stage Placement
Implant sites were determined using a surgical guide and the CT Scan, and the osteotomies were performed according to the manufacturer's protocol. The graft material was placed and condensed carefully against the medial and anterior wall of the sinus cavity. The implants were then placed in their corresponding osteotomies and sinus packed with additional bone graft to completely cover the implants and the buccal window osteotomy.
Delayed or 2 Stage Placement
The same procedure was performed but the implants were not simultaneously placed. The graft was placed and allowed to heal for 6 to 9 months.
At the 6 to 9 month follow-up visit, a panoramic or CT scan was obtained to assess total bone height before implant placement. Implant placement was performed after the same procedure as in the 1 stage procedure, under local anesthesia in conjunction with a surgical guide. The administration of antibiotic prophylaxis (amoxicillin 2000 mg or clindamycin 600 mg, depending on the history of drug allergy) 1 hour before surgery was given to the patients.
For both protocols, after completion of sinus grafting, the lateral wall osteotomy was covered by using PRGF (Fig. 2D). In 3 sinus procedures a collagen membrane was used to cover the replaced bone wall (Bio-Guide; Geistlich Pharma, Wolhusen, Switzerland).
The flap was coronally advanced and was sutured without tension using polyglactin 910 (Vicryl; Ethicon Inc., Cincinnati, OH) or chromic gut sutures (Chromic gut; Ethicon Inc., Cincinnati, OH).
The postsurgical care after the SAP was similar to standard SAP procedures.22 Patients were continued for 7 to 10 days of antibiotic coverage with the same one taken preoperatively and prescribed appropriate analgesics. In addition, a chlorhexidine mouth rinse (0.12%) was prescribed for twice daily for 14 days. The patients were also instructed to avoid chewing on the treated area. Patients returned for postoperative follow-up at one week and for any remaining suture removal 2 weeks after the surgery. Patients were seen at regular intervals during the healing period (6–9 months), at one and 3 months after initial surgery.
Relief of the temporary, fixed, or removable prosthesis (when present) over the edentulous area was performed before insertion of the provisional after the surgery.
The provisional prosthesis was made of metal and composite resin. After a healing period of 6 to 12 months, final impressions were taken, depending if implants were placed at stage 1 or stage 2. Patients were provided with a fixed implant-supported final prosthesis which was placed 15 months after implant placement. Before final delivery, radiographs were taken to verify the adequate fit and adaptation of the abutment-implant interface. The majority of implants were splinted (n = 201) and screw retained (n = 160). Occlusal adjustment was performed at the time of delivery of the final restoration. After the placement of the final prosthesis, all patients were enrolled in a program consisting of professional maintenance, oral hygiene instructions, and periodic evaluations at 1, 3, 6 months, 1 year, and once every year the afterward.
Eighteen implants were immediate loaded with screw-retained temporary fixed partial provisional restorations on the day of surgery. During surgery, implant level impressions and bite registrations were taken and delivered to the dental laboratory. Based on the diagnostic wax-up and articulated casts, resin temporary prostheses with titanium reinforcement were fabricated in the dental laboratory. The provisional prostheses were screwed over the implants on the same day of the surgery. In case of multiple partial edentulism, all the implants were splinted. A total of 21 implants were immediate loaded at stage 2 surgery. After a minimum of 6 months after implant placement, the final impression was made to obtain a master cast on which the final fixed implant-supported prosthesis was fabricated (Fig. 3).
The data were recorded including the survival and success parameters as described by Misch et al23 and Albrektsson et al.24 An implant was considered as surviving if it was still in function without complications such as pain, swelling, and mobility. Implant failure was considered as any implant lost due to any cause, either biological (failure to establish osseointegration or advanced periimplantitis) or biomechanical.25 A failure was considered as early if it occurred before final prosthesis placement, and late if it occurred afterward.
Information related to patient was collected to analyze demographic data (age and gender distribution), social habits (smoking habits), history of periodontal disease, and history of sinusitis. Then, information related to implant details (implant brand, implant diameter, implant length, and insertion torque/primary stability), surgical technique (graft material, initial residual bone height, time of implant placement [stage 1 vs stage 2]), type of prosthesis (screw-cemented, immediate loading/delayed loading, split/non-split), and complications, were also recorded for each patient.
The primary outcome was implant failure time (in months). To identify strong predictors of implant failure, Kaplan-Meier plots were generated of sociodemographic and behavioral characteristics such as age, sex, and current smoking status. Clinical parameters such as history of periodontal disease and sinusitis were also assessed. Implant-specific variables including implant dimensions, residual bone height, complications, time of implant placement (stage 1 vs stage 2), and time of loading were analyzed.
Cox proportional hazards regression models were constructed using the frailty approach for clustered failure-time observations with robust variance-covariance estimators. This approach uses a random-effect term (bi) which accounts for within-patient correlation because of unobserved common covariate data, and has therefore been recommended for use with studies involving correlated survival observations such as dental implant failure.26 The proportionality assumption was confirmed by inspection of adjusted log (−log [survival]) curves and examination of time-dependent covariates. Unavailable and multivariable hazard ratios (HRs) and frailty robust P values were reported. Statistical analyses were conducted with the SAS 9.3 statistical software package (Cary, NC).
Table 1 shows the distribution of sociodemographic and clinical characteristics of the patient population. There were a total of 67 patients with a mean age of 56 years. These included 37 females and 30 males. Of those patients, 13.4% were current smokers and a majority (68.7%) had a history of periodontitis. Those with history of radiotherapy or chemotherapy and pregnant woman were not found among the patients included.
A total of 217 implants were inserted. Table 2 shows sinus/implant-related characteristics. Thirty-one patients underwent bilateral maxillary SA. Patients were followed for a mean period of 85.87 months, SD: ±43.80 months from the time of implant placement (163 implants were followed up for 5 years or more, whereas 54 implants were followed up for less than 5 years). One hundred and forty implants were placed simultaneously (stage 1), and 77 implants were placed with a stage 2 procedure in a mean of 11.99 months after sinus grafting. Eighteen implants in the one stage procedure (in 7 patients) were immediate loaded and 3 of the implants failed in a mean of 2.33 months. Among implants placed in a 2 stage procedure, 21 implants (5 patients) were immediate loaded, and 6 of these implants failed (71% survival).
Table 3 depicts characteristics of implant complications. A total of 195 implants were successfully integrated, with a total of 89.9% cumulative survival rate. (Figs. 4 and 5). In all cases, bone augmentation was achieved after sinus grafting allowed implant placement with primary stability. Of a total of 22 implants, 15 failed in patients showing implant mobility in a mean period of 7 months (range:1–130 months). Of these, 77.3% (n = 17) were considered as early failures (within the first 2 years of implant placement) because of the inability to establish osseointegration, and the remaining 22.7% (n = 5), within 6 to 10.83 years, as late failures because of advanced periimplantitis. The implant failure rate among BTI implants was 9.14% (15 of 164) in 15 patients (6.9%), whereas 13.2% (7 of 53) were among Nobel implants in 7 patients (3.2%). Regarding bone grafting material, an implant failure rate of 10% was found among ABBM+PRGF+autogenous (2 of 20), and 10% among ABBM+PRGF (20 of 197).
Associations between patient characteristics and implant failure were examined in univariable Cox regression models (Table 4). Whereas history of periodontitis was a significant predictor of implant failure (Fig. 6; logrank P = 0.0008), HRs could not be estimated because all of the failures (events) occurred in patients with a history of periodontitis. Of the demographic and behavioral characteristics examined, smoking was the only marginally significant predictors. Current smokers had about 3-fold higher hazard-risk of implant failure than noncurrent smokers (HR = 2.92, 95% confidence interval [CI] = 1.18–7.23). When adjusted for implant characteristics and other demographic factors in Table 4, the association between smoking and implant failure strengthened (HR = 2.32, 95% CI: 0.67–8.06).
When implant-related characteristics were considered, preoperative residual bone and postoperative implant loading were the only statistically significant predictors of implant failure in univariate analysis. Implants that were immediate loaded had a 4- to 6-fold higher hazard-risk of implant failure compared with those with delayed loading (HR = 4.65, 95% CI: 1.92–1.26).
Implants with a delayed time of implant placement had a 2- to 3-fold higher hazard-risk of failure compared with implants with a simultaneous time of implant placement (HR = 2.37, 95% CI: 1.02–5.50).
Considering crestal bone height, 55% reduction in hazard-risk of failure was observed comparing 3–5 mm with <3 mm, and an 86% reduction comparing ≥5 mm with <3 mm (P for trend = 0.0017).
Implant length and width were found to be similarly strong, albeit nonstatistically significant, predictors of implant failure. For instance, compared with individuals with implant lengths of 10 to 12 mm, there was a 21% lower hazard-risk of implant failure among those with <10 mm implant lengths (HR = 0.79, 95% CI: 0.18–3.46), and 63% lower risk of failure with >12 mm lengths compared with those of 10 to 12 mm lengths (HR = 0.37, 95% CI: 0.14–1.03). A similar association was found with implant widths of <4 mm as compared with those of 4 to 4.5 mm.
In multivariable analyses, the associations of implant length, residual bone height, and time of implant loading with implant failure were found to be strengthened, with preoperative residual bone height and time of implant loading as the only statistically significant predictors. To construct a parsimonious multivariable model (Table 5), we retained the predictors of implant failure that achieved a P value of ≤0.10; namely, implant length, residual bone height and time of loading. Residual bone height and time of loading remained the strongest predictors of implant failure, after adjustment for each other. In sensitivity analyses, the parsimonious multivariable model was further adjusted by history of periodontitis and found that the estimates did not appreciably change from those reported on Table 5.
Only 5 Schneiderian membrane perforations were observed in the 100 sinuses that underwent surgery, resulting in an overall perforation rate of 5.0%.
To our knowledge, this is the first long-term retrospective cohort study to report on implant survival in patients receiving PRGF in conjunction with a maxillary sinus lift. Significant improvements in implant survival with increased residual bone and implant length were found. Moreover, immediate loading of implants showed significantly higher risks of implant failure than those with delayed loadings. These associations were independent of sociodemographic/behavioral characteristics including smoking.
This study had some notable limitations. First, sufficient numbers (and limited power) to detect differences across finer strata of several characteristics limited the findings. Second, risk factors such as poor oral hygiene, diet, alcohol consumption that may additionally predict implant survival were not assessed. Nevertheless, this study represents the first attempt to evaluate sociodemographic/behavioral and clinical predictors of implant survival in cases of SA with PRGF. Moreover, the results may be clinically significant, because a large number of procedures were analyzed for a follow-up time of up to 165 months.
Of the 217 implants investigated in this study, 22 were lost, with an overall implant survival rate of 90% during the follow-up period. This result is slightly lower than that was previously reported which showed 100% implant survival with a mean follow-up of 33 months after sinus floor augmentation surgery with PRGF technology.18 It is noticeable that implant survival reported in this study is comparable with that from studies describing the use of bone substitute material without addition of growth factors including previous systematic reviews of the literature with an overall implant survival rate above 90%.4,6,27,28 In a systematic review carried out by Del Fabbro et al7 regarding implant survivals, the authors concluded that no evident benefit of the use of platelet concentrates can be drawn from the included studies. Furthermore, a recent systematic review reported that the implant survival rate with SAP using a lateral wall varied from 75.6% to 100% with a mean follow-up from 3 to 7 years.29
Of the 22 lost implants, 17 were lost before the end of the first year after implant placement and the remaining 5 within 6 to 9 years. This result may suggest that the causes of early loss of implants could be different from the causes of late implant failures.30 The failures that occurred during the first year were related to failure to establish osseointegration, possibly related to surgical procedures or patient-related factors. Late failures were caused by biological complications such as periimplantitis.
Some studies have reported beneficial outcomes when a platelet-rich product was combined with different bone substitutes for SAP.31–35 In this study, a combination of ABBM and PRGF was employed as graft material in 92 of the 100 sinuses and ABBM + PRGF + Autogenous bone in 8 sinuses (of 100). However, limited information is currently available regarding the influence of using PRGF in combination with this bone substitute on the outcomes following SAP.18,36,37 It must be emphasized that the use of PRGF offers many important advantages for SA.18 These advantages include reduced tissue inflammation after surgery, increased bone formation, promoting the vascularization of bone tissue and higher values of bone density.17,18,38 In the study by Anitua et al,36 radiographic evaluation of bone density using the Hounsfield scale also revealed significantly higher values for cases in which PRGF was used as compared with those grafted with anorganic bovine bone alone.
The use of PRGF also facilitates the handling, manipulation, and administration of the graft particles, and increases the overall volume of the graft by improving the osteoconductive properties of the ABBM.18,37 PRGF was especially interesting in cases of membrane perforation and to cover the lateral wall after grafting. However, the analysis of histomorphometric data suggested that these advantages may be more important during the initial healing process (3–6 months) than long-term outcomes.7,19 This suggested additional regenerative potential provided by platelet-derived growth factors during the early healing phase could reduce the time elapsing between grafting and implant placement and loading, providing a significant reduction of the total treatment time.19
Immediate loading in the posterior maxilla following SAP is particularly controversial. Few studies have been published on immediate loading in the posterior maxilla, because of the low bone density, reduced bone volumes, and risk of low primary stability.39–42 However, previous authors have suggested that immediate loading is applicable for implants placed in previously augmented sites.43,44 This study reported a reduced implant survival with the immediate loaded implants. This result of this study suggests that immediate loading may play a significant role in implant failure after SAP. However, a recent study of the maxillary sinus membrane elevation with simultaneous placement and immediate loading showed high implant survival rate (100%) after 2 years of loading.42
The influence of implant placement timing (simultaneous SAP and implant placement vs a delayed protocol) is also controversial. Reported survival rates of implants placed in conjunction with a grafting procedure range from 61.2% to 100% (96.5% in this series) and from 72.7% to 100% with the delayed approach.15,45 These 2 approaches seem to result in similar outcomes27; consequently, the selection of one approach or the other has been normally driven by the clinician according to the quantity and quality of bone in the residual maxilla.
This study showed differences in implant survival rates between patients with RBH ≥ 3 mm and those with RBH < 3 mm. Different studies showed that sinus with a RBH < 3 mm had a slightly higher risk for implant failures.46–48 However, previous studies supported the hypothesis that if the initial bone height allows primary implant stability, simultaneous (stage 1) implant placement may be considered regardless of RBH, with the advantage of reducing treatment time.49,50 In this regard, the clinician's decision may depend on the primary implant stability regarding the loading protocol and establish the healing time.51
In this study, all SAPs were performed with the lateral window approach by using a piezoelectric surgical device. This method has been regarded as useful to avoid sinus membrane perforation.52,53 Only 5 sinus membrane perforations were observed in the 100 sinuses that underwent surgery, resulting in an overall perforation rate of 5.0%. This finding is in agreement with that of other studies that used piezoelectric surgery to perform SAP and that reported similar perforation rates.52,54
This study had some limitations related to study design. Disadvantages may lay in certain degrees of variability in clinical parameters such as probing depth, bleeding on probing, recession, patients' satisfaction, marginal bone loss around implants and control group, which were not included in this study because of the nature of the study design and information available. Furthermore, prospective controlled randomized clinical trials are necessary to support the results of this article.
In summary, this study showed that the use of PRGFs in combination with a bone substitute graft for maxillary sinus grafting is a technique with low surgical morbidity that allows implant restoration or the edentulous atrophic posterior maxilla. Longer implant length and residual bone height were significantly correlated with implant survival, whereas immediate implant loading and smoking habit were significantly associated with implant failure. Prospective randomized clinical trial, however, is needed to confirm the findings in this study.
The authors claim to have no financial interest, either directly or indirectly, in the products or information listed in the article.
The authors also thank Dr. José Pardiñas Arias (JPA), Dra. Carmen López Prieto and Ms. Isabel Fontanes. The authors would also like to thank Dr. Christopher Salazar for his support during the statistical analysis.
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