Influence of graft quality and marginal bone loss on implants placed in maxillary grafted sinus: a finite element study

Abstract

The purpose of this study was to investigate the biomechanical effects of graft stiffness and progression of marginal bone loss (MBL) in the bone surrounding an implant placed in a maxillary grafted sinus based on the finite element method. The simulating model of graft stiffness as well as depth of MBL was varied to simulate nine different clinical scenarios. The results showed that the high-level strain distributions in peri-implant tissue increased with the increase in MBL depth when the stiffness of the graft was less than that of the cancellous bone (less stiffness graft models). The strain energy density (SED) value showed that a slight MBL depth (1.3 mm) with medium stiffness of grafted bone can reach the optimal load sharing due to the exhibited similar values of SED in the crestal cortical, cancellous, and grafted bone. With progression of MBL and the decrease in graft quality, maximal displacement of the implant increased considerably. Our results demonstrated that the effects of the two investigated factors (progression of MBL and graft stiffness) on the biomechanical adaptation are likely to be interrelated. The results also reveal that for clinical situations with poor grafted bone quality and progression of MBL, it is critical to consider implant stability.

Introduction

Studies have shown that the stability of implant is related to the biomechanical properties of the bone surrounding [5, 20, 30, 33]. The structures of bone around implants placed in maxillary grafted sinus are complex, as shown in the cone beam CT (CBCT) images (Fig. 1). Several sinus bone graft augmentation techniques have been developed using various graft materials [22]. The incidence of implant loss in the posterior maxilla is varied from 2 to 54%, depended on the graft used [26]. Moy et al. suggested that the graft quality ultimately achieved after sinus graft healing is biomechanically predetermined by the density of the natural bone in that location [20]. However, the contribution of the grafted bone in establishing and maintaining implant stability is not yet well known. Previous studies have suggested that load-bearing characteristics of grafted bone depend on the graft material and its maturation process [25].

Fig. 1

Cone beam CT images representing the complex structure of an implant placed in a maxillary grafted sinus: a bucco-palatal view, b mesio-distal view, c measurement of marginal bone level, and d graft quality (444.05 ± 154.62 HU)

Time-dependent marginal bone loss (MBL) around implants is still unavoidable and could jeopardize implant stability and the supported prosthesis [8, 10]. The outcome of comparative clinical research on different implant systems reported analogous MBL per year [8, 17]. Smoking, small implant surface area and a delayed implantation approach were related to enhance MBL around dental implant placed in maxillary grafted sinus [8]. Bone loss usually begins at the crestal area of the cortical bone and can progress toward the apical region. Clinically, bone loss ranging between 1 and 2.6 mm has been reported to occur around the neck of successfully integrated implants [16, 19, 32].

Several biomechanical studies have investigated the biomechanics of bone surrounding implants placed in the posterior edentulous maxilla with sinus graft [5, 6, 30]. These studies analyzed the effect by varying different parameters of the graft, implant, and/or supra-structure in the finite element model (FEM) without considering progression of MBL. From the biomechanical point of view, it is not known in such cases whether the graft or residual bone secured the implant which placed in maxillary grafted sinus.

The intent of the study presented here was to investigate the biomechanical performance of bone around implant placed in maxillary grafted sinus based on the progression of MBL and variations in graft stiffness that could simulate the possible clinical scenarios related to several investigations [6, 11, 12, 25]. The components in an osseointegrated implant placed in maxillary grafted sinus are complex geometry. We, therefore, simplified to the geometrical model that could represent the biomechanical behavior of complex peri-implant system with progression of MBL [27]. Strain distribution, strain energy density (SED), and implant displacement were observed as the biomechanical indicators for this study.

Methods

Finite element model

A three-dimensional CAD model of a standard osseointegrated implant was designed and placed in the maxillary grafted sinus. The geometry of the maxilla was defined by a bucco-palatal section. The unilateral edentulous posterior maxilla with grafted sinus model consisted of native bone and graft material of 14 mm in height, 11 mm in bucco-palatal width, and 15 mm in mesio-distal length. The total height of the native bone component was 5 mm, consisting of 1-mm crestal cortical bone, 3.5-mm cancellous bone, and 0.5-mm sinus cortical bone (Fig. 2a, d) [6]. The bone graft component had a total height of 9 mm. The grafting morphology was considered to be complete peri-implant packing as suggested by Tepper et al., which was considered to be an ideal case [30]. Progression of MBL varied in depth (from 1.3 to 2.6 mm), as models were simulated for analysis (Fig. 2b, c) [12].

Fig. 2

Schematic drawing representation of the study models in the bucco-palatal section. a non-MBL, b 1.3-mm MBL, c 2.6-mm MBL, d configuration of the complex system model, e finite element model and the oblique loading

In order to simplify the analysis, the model of the implant and the abutment was modeled as a unit; the porcelain fused to gold alloy crown was created on top of the abutment. The standard Straumann implant (Institut Straumann AG, Waidenburg, Switzerland) employed in the model was 3.75 mm in diameter and 11.5 mm in total length. The graft stiffness and depth of MBL were varied to simulate nine different clinical scenarios as shown in Table 1.

Table 1 Study models designed for biomechanical performance analysis

The FEM was developed using MSC Patran (MSC Software, Inc., USA). The analyses were done through MSC Marc (MSC Software, Inc., USA). The model was meshed with 4-node tetrahedron elements (Fig. 2e). A finer mesh was generated around the implant. Models were composed of elements varying from 113,341 to 118,728 and nodes ranging from 27,500 to 28,330.

Applied boundary conditions and implant loading

In order to simplify an ideal osseointegration, the grafted bone and implant were united together. The implant was rigidly anchored in the bone model along its entire interface. The same type of contact was provided at the crown–abutment interface. Oblique load was considered in this study as it mimics the masticatory pattern more realistically and generates considerable localized stress in the bone [9]. A functional loading force of 100 N was applied to the occlusal node at the center top surface of the superstructure. A defined force inclined to the posterior by 30° relative to the implant axis (Y-axis) and by 30° away from the sagittal plane (Z-axis) (Fig. 2e) [1, 30].

Material properties

The properties of the materials used in the study are listed in Table 2. All the values for the modulus of elasticity and Poisson’s ratio were kept constant throughout the testing, except the grafted bone, to simulate the different quality of graft stiffness (low, medium, and high). All the materials used in the model were assumed to be isotropic, homogenous, and linearly elastic.

Table 2 The properties of the materials used in the study [3, 6, 21, 25, 28, 29]

Results

Strain distributions

As shown in Fig. 3, the strain distribution patterns are shown as contour lines with different colors to represent bone deformation after implant loading. The results showed that the high level of strain distributions had increased when the graft stiffness had decreased. Furthermore, the high level of strain distributions increased with the increase in MBL depth when the stiffness of the graft was less than that of the cancellous bone (less stiffness models). This result indicated that the progression of MBL had a biomechanical effect especially in the case of less-stiff grafted model as compared to medium and high-stiff grafted models.

Fig. 3

Equivalent of total strain distributions in peri-implant tissue

Strain energy density (SED)

The SED is an important indicator to evaluate the biomechanical performance of energy absorption or load sharing in different properties of peri-implant tissues as shown in Fig. 4a. The results as shown in Fig. 4b indicated that the maximum SED values exhibited in the graft portion tend to increase when the graft stiffness increases. Regarding the progression of MBL, the SED values in the slight MBL model (1.3-MBL) exhibited in the crestal cortical bone had decreased as compared to the non-MBL model. However, in the high progressive MBL model (2.6-MBL), the SED values exhibited in the crestal cortical bone had increased as compared to the non-MBL and 1.3-MBL models. If this trend of MBL progresses continuously, this would lead to implant instability.

Fig. 4

The SED distribution in each portions of 1.3-MBL medium model (a), the maximum of SED value in all simulating models (b)

Considering the result of SED in the term of load sharing aspect of all simulating models, it was found that the SED values in the 1.3-MBL with medium graft stiffness model had exhibited the optimal load sharing in the peri-implant tissue due to similar values of SED in crestal cortical, cancellous, and graft portions (Fig. 4b). These findings suggest that the progression of MBL and the variation of graft stiffness are interrelated in reflecting the load sharing in peri-implant tissue.

Maximum displacements of implant

As shown in Fig. 5, it was found that the progression of MBL and the variation of graft stiffness affected to the displacement of implant. The trend of maximum displacement of implant had increased when the progression of MBL had increased. Regardless of the MBL progression, the maximum displacement of implant had slightly decreased when the graft stiffness had increased (Fig. 6). The magnitude of implant displacement showed that with the progressive MBL and the decrease in graft quality, maximal displacement of the implant increased considerably.

Fig. 5

FE models of the displacements of the implant

Fig. 6

Maximum displacement values of implant placed in the variation of graft stiffness and MBL depths

Discussion

The FEM of complex structure in this study was developed similar to previous study [6]. In order to exclude the influences of anatomical variations of bone as suggested by Akca and Cehreli [1], we decided not to use an anatomical model of jawbone provided by CBCT data. Rather, a dimensional simplify FEM of a posterior maxilla with grafted sinus has been developed in this study. In order to report detected bone loss, previous studies on thread implants have used the thread pitch as a unit of study [10]. In this study, we simulated the MBL progression levels by decreasing in increments of 1.3 mm. This level was equivalent to several implants of many implant systems [12].

The graft quality can vary depending on many factors such as the density of the natural bone, graft materials, or maturation process. It is, therefore, difficult to predict the clinical outcome of osseointegrated implant after functional loading. Currently, CBCT data from the clinical cases can be integrated with an advanced medical imaging to illustrate the marginal bone level (Fig. 1c). The bone density of the interesting area is displayed in Hounsfield Units (HU) [13–15, 23]. For example, the bone density of the selected area in the posterior maxilla is 444.05 + 154.62 HU (Fig. 1d), which is comparable to the previous report [31]. Many authors had investigated using clinical observations and computational mechano-biological modeling procedures that described the biomechanical status of bone surrounding implants in function [2, 24, 33]. In our study, we used the advantages of three-dimensional FEM to simulate the variation of graft stiffness and the progression of MBL. Thus, the strains distribution, SED, and maximum displacement of implant in the bone surrounding implant were observed.

Load-bearing capacities

Cehreli et al. demonstrated that grafting materials in maxillary sinus, resulting in an enhanced apical portion of implant supported [5]. In our investigation, it was revealed that the quality of graft placed in maxillary sinus plays an important role of load-bearing capacity or adaptability factor to loading related to previous reports [6, 25, 30]. One of the important factor that affected the graft quality is the maturation process such as the bone remodeling [26]. Xu et al. suggested that the reduction in bony area might reflect remodeling of the primary woven bone to stable mature lamellar bone [34]. A change in stiffness overtime was selected to simulate the biomechanical response of either a bone graft maturing overtime as suggested by previous studies [6]. The simulating method in our study yielded results in agreement with previous investigations in terms of the presence of high-level strain increase with lower graft stiffness. An implant placed in poor quality of grafted bone in the sinus might cause increased high-level strains distribution in the peri-implant tissue. This is due to the fact that in the early stage of graft maturation, the loading capacity of grafted bone in the maxillary sinus was lower than that of the native bone (cortical, cancellous) in the posterior edentulous maxilla [24]. It is suggested that the graft quality improves the biomechanical performance of implants placed in maxillary sinus graft. According to the results of the present study, the high-level strain distributions in peri-implant tissue increased with the increase in MBL depth when the stiffness of the graft was less than that of the cancellous bone (less stiffness). These findings suggested that the graft quality improves the biomechanical performance of implants as bone resorption progresses.

Load transferring

Load transferring to surrounding bone is a key factor for the success or failure of a dental implant [7]. Previous study demonstrated that the geometries of bone defect and the physical property of tissues around immediately loaded implant have an impact on mechanotransduction to bone [4]. Our study was designed to evaluate the effects of graft quality and MBL on load transferring to surrounding bone in complex system. Because of a difference between the biomechanical properties in the cortical, cancellous, and graft bone, the SED has been the suitable biomechanical parameter to evaluate load sharing in this analysis [18]. In biomechanical aspect, the osseointegrated implant acts like a bar elastically supported by the surrounding bone. Whatever load applied will be better distributed across the implant and the host bone, the better the bony support of the implant. However, this only applies if all of the host bone surrounding the implant is of identical stiffness [30]. According to our study in complex structure, the SED value is not uniform through the peri-implant tissue but can be concentrated in certain regions depending on graft quality and MBL status. This explains that the slight MBL (1.3 mm) with medium graft stiffness (cancellous bone) simulating model is favorable situation in term of load sharing.

The implant stability

It is difficult to understand how definitive biomechanical factors could cause a displacement of implant after years of function. Acka and Cehreli suggested that the presence of cortical bone noticeably reduced displacement, even in late stages of marginal bone resorption [1]. The important information derived from our study has revealed that the progression of MBL (1.3–2.6-mm) substantially caused more extensive displacements in all graft stiffness. However, through the improvement of graft stiffness during maturation process, the displacement of implant can be reduced. This result indicated that the improvement of the graft quality has a positive effect on the displacement of the implant. It would lead to the implant stability in the maturation stage of graft bone.

Conclusion

Our investigation demonstrated that the effects of the two investigated factors (MBL progression and grafted bone stiffness) on the biomechanical parameters are likely to be interrelated. The findings suggest that the graft quality improves the biomechanical performance of implants as bone resorption progresses and should be used for evaluation of implant prognosis. It is critical to consider the clinical situations where poor grafted bone quality and progression of MBL have been observed.