Effect of Integration Patterns Around Implant Neck on Stress Distribution in Peri-Implant Bone: A Finite Element Analysis Jingyun Han, PhD,1 Yuchun Sun, DMD,2 & Chao Wang, PhD1 1
Key Lab for Biomechanics and Mechanobiology of Education Ministry, School of Biological and Medical Engineering, Beihang University, Beijing, China 2 Peking University School and Hospital of Stomatology, Beijing, China
Keywords Dental implant; finite element analysis; bone resorption; osseointegration; biomechanics. Correspondence Jingyun Han, Beihang University, XueYuan Road No. 37, HaiDian District, Beijing, China 100191. E-mail: [email protected] This study was supported by the National Natural Science Foundation of China (10902010 and 61227902). The authors deny any conflicts of interest. Accepted October 21, 2015 doi: 10.1111/jopr.12434
Abstract Purpose: To investigate the biomechanical performance of different osseointegration patterns between cortical bone and implants using finite element analysis. Materials and Methods: Fifteen finite element models were constructed of the mandibular fixed prosthesis supported by implants. Masticatory loads (200 N axial, 100 N oblique, 40 N horizontal) were applied. The cortical bone/implant interface was divided equally into four layers: upper, upper-middle, lower-middle, and lower. The bone stress and implant displacement were calculated for 5 degrees of uniform integration (0, 20%, 40%, 60%, and 100%) and 10 integration patterns. Results: The stress was concentrated in the bone margin and gradually decreased as osseointegration progressed, when the integrated and nonintegrated areas were alternated on the bone-implant surface. Compared with full integration, the integration of only the lower-middle layer or lower half layers significantly decreased von Mises, tensile, and compressive stresses in cortical bone under oblique and horizontal loads, and these patterns did not induce higher stress in the cancellous bone. For the integration of only the upper or upper-middle layer, stress in the cortical and cancellous bones significantly increased and was considerably higher than in the case of nonintegration. In addition, the maximum stress in the cortical bone was sensitive to the quantity of integrated nodes at the bone margin; lower quantity was associated with higher stress. There was no significant difference in the displacement of implants among 15 models. Conclusions: Integration patterns of cortical bone significantly affect stress distribution in peri-implant bone. The integration of only the lower-middle or lower half layers helps to increase the load-bearing capacity of peri-implant bone and decrease the risk of overloading, while upper integration may further increase the risk of bone resorption.
The introduction of osseointegrated implants symbolizes a turning point in clinical dental practice.1 Due to several advantages, such as being strong, durable, and natural in appearance, dental implants are often considered to be a more appealing option than conventional prostheses. However, preventing marginal bone loss around implants remains a significant challenge. Compared with natural teeth, implants have a lack of periodontal membrane support. The rigid connection with the alveolar bone is harmful to force dispersion. Moreover, cortical bone is about ten times stiffer than cancellous bone.2,3 As a result, cortical bone, although notably thin, plays a major role in the mechanical competence of implant anchorage.4 Excessive masticatory loads have been blamed for marginal bone loss around implants.5 Miyata et al6,7 observed three times
more bone loss when the controlled occlusal overload was produced by a superstructure in monkeys. Isidor8 and Ferrari et al9 reported breakdown of the crestal bone and the loss of osseointegration under nonaxial overloading in animal studies. Nagasawa et al10 established an implant occlusion model using rats, and revealed degenerative changes in osseointegration and/or in the peri-implant bone upon excessive loading. In addition, some clinical literature presents a positive correlation between high occlusal load and marginal bone loss.11,12 Pera et al13 and Zweerset al14 found that tapered implants and a wider implant diameter, which meant a decrease in bone stress15,16 , resulted in less marginal bone loss. Therefore, improving load transmission to decrease the stress level in marginal bone is a critical problem for osseointegrated implants.
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
1
Effect of Osseointegration Patterns on Bone Stress
Han et al
Figure 1 Cross-sectional view of FE models: (A) mandible segment with a dental implant and crown; (B) distribution of integrated layers.
Table 1 Material properties of the implant, crown, and cancellous bone Material Ti-6Al-4V implants Gold alloy crown Cancellous bone
Young’s modulus (MPa)
Poisson’s ratio
110,000 90,000 3000
0.35 0.3 0.3
Finite element (FE) analysis (FEA) has been an effective tool for studying the biomechanical problem of implantation.17-19 The quality of the bone/implant interface, such as integration percentage and patterns, may greatly affect stress distribution in peri-implant bone. Han et al and Lu et al constructed 3D FE models of implants, and concluded that the bone stress gradually decreased as osseointegration progressed.20,21 Papavasiliou et al and Xing and Liu designed five types of osseointegration patterns (locally alternating, coronal only, apical only, facial only, and lingual only) on the bone/implant interface at 50% osseointegration. Results showed that coronal integration decreased both crestal and apical stress, while the apical pattern induced higher apical stress.22,23 Additionally, regardless of osseointegration quality, implant shapes, and loading angle, a general rule in stress distribution emerges: cortical bone bears most of the masticatory load, and stress concentration occurs in the cortical bone margin.24,25 Accordingly, we proposed that changing osseointegration patterns, specifically on the cortical bone interface as opposed to the whole bone/implant interface, may be more favorable for homogeneous stress distribution and a lower stress magnitude. The purpose of this study is to develop 3D FE models of the single mandibular fixed prosthesis supported by implants and to evaluate the biomechanical performance of the different osseointegration patterns on the cortical bone/implant interface. Thus, these results may provide the theoretical basis for optimizing implant design and decreasing the risk of overloadinduced bone resorption.
Materials and methods The FE models consisted of four parts: cortical bone, cancellous bone, implant, and crown (Fig 1). A bone block ofthe mandible in the second premolar region was constructed based on the CT 2
image of an adult male patient. The cortical bone had a thickness of approximately 2 mm. Based on reverse engineering, a 4.1*12 mm screw-type dental implant and crown were reconstructed in commercial CAD software (Geomagic Studio, v8.0, Raindrop; Geomagic, Inc., Morrisville, NC) and I-DEAS (v.10.0, EDS, Plano, TX). All geometric models were meshed with 10-node tetrahedron elements. For sufficient accuracy in each case, a convergence test was performed to determine the number of elements. The convergence rate was less than 1% for stress and less than 0.5% for displacement. In total, the models consisted of 69,388 elements and 111,901 nodes. The material properties of implants, crown, and cancellous bone were assumed to be isotropic, homogeneous, and linearly elastic (Table 1).26,27 The cortical bone was represented by the anisotropic material model (Ex = 17 GPa, Ey = 13.8 GPa, Ez = 10.6 GPa; Gxy = 6.2 GPa, Gyz = 4.1 GPa, Gxz = 5.4 GPa; vxy = 0.38, vyz = 0.23, vxz = 0.47).28 Masticatory forces of 200 N, 100 N, and 40 N were applied to the center of the crown axially (AX), buccolingually (BL), and horizontally (HZ), respectively.29-31 The mesial and distal surfaces of the mandibular bone were constrained in x, y, and z directions (displacements = 0). Two contact types, “frictional contact” and “bonded contact,” were defined on the bone/implant interface. “Frictional contact” indicated a nonintegrated state and enabled frictional sliding (frictional coefficient, µ = 0.3).32 “Bonded contact” meant an integrated state, and there was no relative sliding and separation between implants and bone. In this study, the cancellous bone/implant interface was assumed to be bonded together perfectly. For the cortical bone, the different integration patterns were considered to simulate the following case. Model case 1: localized integration patterns (LIP)
The cortical bone/implant interface was divided equally into four layers along an axial direction: upper, upper-middle, lower-middle, and lower (Fig 1B).The localized integration patterns with different osseointegration percentages (OIP) were designed on the cortical bone/implant interface (Table 2). In the first type of model, only one of the four layers was
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
Han et al
Effect of Osseointegration Patterns on Bone Stress
Table 2 Model names with different integrated patterns Models
Region of localized integration
UIP
LIP 40-I LIP 40-II LIP 40-III LIP 40-IV LIP 60-V LIP 60-VI LIP 20-I LIP 20-II LIP 20-III LIP 20-IV
Upper layer Upper-middle layer Lower-middle layer Lower layer Upper and upper-middle layers Lower-middle and lower layers Upper layer Upper-middle layer Lower-middle layer Lower layer
40% 40% 40% 40% 60% 60% 20% 20% 20% 20%
60%. In the third type, only one of the four layers was designed as the integrated area, and the quantity of the bonded nodes was decreased by half. The total OIP was approximately 20% on the cortical bone/implant interface. In this study, the different models were named according to a combination of pattern types, OIP, and integrated layer (Table 2). The model of full osseointegration (OIP 100%) was the control, and a comparative analysis was performed to evaluate the effect of LIP on bone stress and implant displacement.
Model case 2: uniform integration patterns (UIP)
designated as the integrated area, while the other layers were the nonintegrated areas. The total OIP was approximately 40% on the cortical bone/implant interface. In the second type, only the upper half or only the lower half interfaces were defined as the bonded contacts, and the total OIP was approximately
UIP was used to simulate random osseointegration in cortical bone. The integrated and nonintegrated areas alternated on the cortical bone/implant interface. Five FE models with different OIPs (100%, 60%, 40%, 20%, 0) were constructed. For the UIP, a comparative analysis was performed to evaluate the effect of OIP on bone stress and implant displacement.
Figure 2 Von Mises stress distribution of the cortical bone in the LIP models with 40% OIP: (A) axial loading, (B) buccolingual loading, (C) horizontal loading.
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
3
Effect of Osseointegration Patterns on Bone Stress
Han et al
Figure 3 Von Mises stress at the cortical bone margin in the LIP models with 40% OIP: (A) axial loading, (B) buccolingual loading, (C) horizontal loadingand, (D) path.
Results
Table 3 Maximum von Mises stress in cortical and cancellous bone (MPa)
Von Mises stress in the cortical bone
In the LIP models with an OIP of 40%, the von Mises stress distribution in the cortical bone is shown in Figure 2. A similar stress concentration was observed in the models of LIP 40-I and LIP 40-II compared with the model of OIP 100%, and the maximum stresses were located in the cortical bone margin. By contrast, the stress distribution was more uniform in the LIP 40-III and LIP 40-IV models, and the starting position of bonded contact became another high stress region in addition to the cortical bone margin. The maximum stresses occurred in the LIP 40-I model. Under axial loading, a marked decrease in cortical bone stress was found, as the integrated region was transferred from layer I to IV. The maximum bone stress was reduced by up to 36.3% in the LIP 40-IV model as compared with the OIP 100% model. Under buccolingual and horizontal loading, the bone stress in the LIP 40-III model was lowest, and decreased by 24.9% and 16.6%, respectively (Fig 3). When OIP decreased to 20% in the LIP models, the highest stress in the cortical bone was located at the starting position of bonded contact. The stress contour plots (Fig 4) showed that the lower the integrated location, the more uniform the bone distribution; however, the LIP of OIP 20% did not improve the stress in the cortical bone, and even engendered higher stress. For example, the stress in the LIP 20-IV model was lowest, and the maximum stress increased by 29.0% to 61.2%, respectively, under buccolingual and horizontal load compared with that in
4
Models
UIP 20% UIP 40% UIP 60% OIP 100%
AX
BL Cortical bone
HZ
44.3 37.9 38.7 39.9
226.3 211.6 200.2 109.0
108.1 76.9 79.0 41.3
Cancellous bone LIP 40-IV LIP 20-III LIP 20-IV UIP 20% OIP 100%
10.38 10.38 10.47 10.59 10.21
23.61 23.16 26.71 22.03 17.45
11.21 11.02 12.72 10.41 8.87
the OIP 100% model. In addition, when OIP increased to 60% in the LIP models, LIP 60-V and LIP 60-VI were similar to OIP 100 and LIP 40-III, respectively, in stress distribution and magnitude. In the UIP models, the maximum stresses were located in the cortical bone margin. The bone stress gradually decreased (Table 3) as OIP increased. Under the same conditions of the OIP, bone stress in the UIP models was significantly higher than in the LIP models.
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
Han et al
Effect of Osseointegration Patterns on Bone Stress
Figure 4 Von Mises stress distribution of the cortical bone in the LIP models with 20% OIP: (A) axial loading, (B) buccolingual loading, (C) horizontal loading.
Von Mises stress in cancellous bone
The bone stress distribution was highly similar in all models. The stress concentration primarily occurred in the following areas:
r r r
The lingual side adjacent to the cortical bone, the first and last threads, and the apical area under AX The top adjacent to the cortical bone and the first threads under BL The lingual side adjacent to the cortical bone and the first threads under HZ
Under AX, a slight change in stress was observed in all models. Under BL and HZ, stress significantly increased in the LIP 40-IV, LIP 20-III, LIP 20-IV, and UIP 20% models compared with the OIP 100% model (Fig 5, Table 3). The biggest difference occurred in the LIP 20-IV model, and the
maximum stress increased by 53.2% and 36.6%, respectively, under BL and HZ. Principal stress in peri-implant bone
In the LIP models with OIP at 40%, the principal stress distribution in the cortical bone is shown in Figure 6 and 7. The stress concentration occurred at the start site of bonded contact. Compared with the OIP 100% model, the LIP models increased the maximum principal stress under AX (Table 4), but the maximum principal stress under BL and HZ and the minimum principal stress significantly decreased in the LIP 40-III and LIP 40-IV models. In cancellous bone, the stress concentration was located at the top side adjacent to the cortical bone, the first threads, and the apical area. Under AX, there was no significant difference in principle bone stress between the full integrated model and
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
5
Effect of Osseointegration Patterns on Bone Stress
Han et al
Figure 5 Von Mises stress distribution in the cancellous bone: (A) axial loading, (B) buccolingual loading, (C) horizontal loading.
the LIP models with OIP at 40% (Table 4). On the contrary, the principal stress gradually increased as the bonded contact moved to the lower position under BL and HL. The biggest difference in stress was observed in the LIP 40-IV model, and 6
the maximum tensile and compressive stress increased approximately two times and 48.8%, respectively. In addition, the LIP models with OIP at 20% were similar to the models of LIP with OIP at 40% in bone stress
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
Han et al
Effect of Osseointegration Patterns on Bone Stress
Table 4 Maximum tensile and compressive stress in cortical and cancellous bone (MPa) AX
OIP 100% LIP 40-Ⅰ LIP 40-Ⅱ LIP 40-Ⅲ LIP 40-Ⅳ
+9.9/–58.4 +20.0/–61.9 +37.9/–37.8 +33.7/–31.6 +37.9/–29.7
BL Cortical bone
HO
+153.8/–155.2 +164.5/–163.2 +124.1/–100.7 +88.5/–90.1 +84.9/–91.6
+61.0/–67.9 +65.8/–71.4 +46.6/–42.2 +39.2/–38.1 +52.1/–38.9
Cancellous bone OIP 100% LIP 40-Ⅰ LIP 40-Ⅱ LIP 40-Ⅲ LIP 40-Ⅳ
+12.5/–12.4 +12.9/–12.7 +12.8/–12.8 +12.9/–13.1 +13.2/–13.6
+6.2/–6.4 +6.7/–6.7 +8.2/–7.5 +10.3/–8.6 +12.8/–10.4
+3.5/–4.1 +3.9/–4.6 +4.7/–4.6 +5.8/–5.3 +7.2/–6.1
Table 5 Maximum implant displacement (µm)
OIP 100% LIP 40-I LIP 40-II LIP 40-III LIP 40-IV LIP 20-I LIP 20-II LIP 20-III LIP 20-IV LIP 60-V LIP 60-VI
AX
BL
HO
6.26 6.28 6.35 6.76 6.85 6.37 6.40 6.49 6.56 6.27 6.43
16.48 16.62 17.25 18.26 19.34 17.63 18.13 19.11 19.99 16.49 18.24
10.12 10.21 10.53 11.09 11.68 10.76 11.03 11.56 12.04 10.13 11.02
distribution, but there was higher stress in the peri-implant bone under BL and HL in the LIP models with OIP at 20%. The models of LIP 60-V and LIP 60-VI were similar to OIP 100% and LIP 40-III, respectively, in stress distribution and magnitude. Displacement of implants
The maximum displacement occurred on the implant neck adjacent to the bone margin. There was a slight difference between the full integrated model and the LIP models (Table 5). It was determined that a lower osseointegration location and OIP could induce higher displacement of implants. Accordingly, the maximum displacement was observed in the LIP 20-IV model.
Discussion Stress concentration in marginal bone has been suggested to be a direct cause of bone resorption and osseointegration failure.15,33 Many studies have tried to optimize implant material properties, implant structure, and surgical procedures to regulate stress levels in the peri-implant bone.24,25,34,35 In the present study, we were more concerned with the biomechanical performance of the cortical bone/implant interface and hypothesized that the
LIP can significantly affect stress distribution in the cortical bone. Accordingly, we developed fifteen 3D FE models with different integrated patterns. In the LIP models with OIP at 40%, the FE results showed that the osseointegration patterns on the cortical bone/implant interface significantly affected the von Mises stress distribution and magnitude in the cortical bone. The bone stress at the start of the bonded contact gradually became comparable to that at the bone margin, as the bonded contact moved to the lower position on the interface of the cortical bone. This meant that the masticatory force was more uniformly transmitted to the cortical bone. As a consequence, the bone stress magnitude significantly decreased compared with that in the model with OIP at 100%, where the integration of only the lower-middle layer or lower half interface occurred. Additionally, principle stress was calculated in the present study.36 We found that the patterns of LIP 40-III and LIP 40-IV could remarkably decrease compressive and tensile stress in cortical bone under BL and HL, and bone tensile stress in the LIP models increased under AX. It is generally known that an oblique and horizontal load is more dangerous than an axial load clinically. The results in this study showed that the bone stress induced by AX was far lower than that induced by BL and HZ, and the data substantiated clinical experience. Overall, the patterns that occurred on only the lower-middle, lower layer, or lower half interface helped to prevent the marginal bone from overloading. To evaluate the effect of osseointegration patterns more comprehensively, models of UIP and LIP with different OIPs were developed. The results showed that the integrated state of the bone margin was a key factor affecting stress level in the cortical bone. When the bone margin completely integrated with the implant, there was no significant difference in cortical bone stress between the full integration and the LIP (e.g., OIP 100% vs. LIP 60-I and OIP 100% vs. LIP 40-I), though the integrated area in the LIP models was lower than in the OIP 100% model. On the contrary, when integration of the bone margin did not occur, the starting position of bonded contact and the number of integrated nodes at the starting position could significantly affect the stress level in the cortical bone. We observed that both conditions were conducive to uniform stress distribution: (1) the starting position of the osseointegration was no higher than the lower-middle layer; and (2) nodes at the starting position were fully integrated. Therefore, the models of LIP 40-III, LIP 60VI, and LIP 40-IV showed better biomechanical performance than the model of full integration. These results reveal that optimization of integration patterns on the cortical bone/implant interface may help improve bone stress distribution more than simply increasing OIP between the bone and implants. Moreover, low OIP at the cortical bone margin would increase the overloading risk of the peri-implant bone. Stress in the cancellous bone has also been of concern in the present study. The results showed that von Mises stress increased when localized integration occurred on the lower layer or when the OIP was very low. In addition, the results showed that principle stress gradually increased as the starting position of localized integration moved to the lower layer. Overall, although the stress in the cancellous bone increased in some LIP models compared with the model of full integration, the largest difference was less than 7.0 MPa. Based on the above data, it
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
7
Effect of Osseointegration Patterns on Bone Stress
Han et al
Figure 6 Tensile stress distribution in the cortical bone: (A) axial loading, (B) buccolingual loading, (C) horizontal loading.
can be observed that stress in cancellous bone is not only far lower than stress in the cortical bone but also far lower than the yield stress of the cancellous bone (53 MPa).37 By contrast, stress in cortical bone has exceeded the yield stress of cortical bone in some models. Accordingly, the results indicate that the risk of overloading in cortical bone is apparently higher than in cancellous bone. Rigid fixation of implants is one of the evaluation criteria for a successful dental implant. Healthy implants should move less than 75 µm during chewing,36 and failure of dental implants could occur if the movement of implants is more than 500 µm. In the present study, the osseointegration patterns affected the displacement of implants, but the maximum difference was less than 4.3 µm between the model of full integration and LIP models. Moreover, the displacement of implants was far lower than 75 µm in all models. Therefore, from a mechanical viewpoint, the osseointegration patterns of the cortical bone/implant interface cannot significantly affect the stability of implants. For the FEA of dental implants, it is important to consider not only axial and horizontal forces but also a combined load
8
(oblique force), because the latter represents a more realistic occlusal direction. Generally, AX is much higher than BL and HZ. Graf et al38 found a ratio of 5:2.5:1 during chewing, and this ratio was used in the present study. Furthermore, it is well known that BL and HZ cause higher torque than AX. Our FE results showed that bone stress under BL and HZ was significantly higher than under AX, especially in the UIP models. Therefore, the results indicate that the case analyses for oblique and horizontal loading should not be ignored in FE models of dental implants, using occlusal adjustment to reduce the oblique or horizontal forces on the premise of a normal occluding relation is recommended for crown design. In the present study, we supported our hypothesis using the FE method, and the results will be verified through a comparison with experimental data in future studies. Additionally, immediate loading has been a more attractive treatment method in the clinic than delayed loading.39 The material property of peri-implant bone varies from soft connective tissue to complete bone maturation during the osseointegration process. The effects of different osseointegration patterns on bone stress are
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
Han et al
Effect of Osseointegration Patterns on Bone Stress
Figure 7 Compressive stress distribution in the cancellous bone (A) axial loading, (B) buccolingual loading, and (C) horizontal loading.
still unclear during different integration phases. Accordingly, this topic will be researched in our future work.
Conclusion Under functional forces, high stress is primarily located in the marginal bone around implants. The osseointegration patterns on the cortical bone/implant interface can significantly affect stress distribution and magnitude in the cortical bone. Compared with full integration, the integrated patterns that occurred only on the lower-middle layer or lower half interface can induce lower von Mises stress, and can significantly decrease compressive and tensile stress in the cortical bone under BL and HL. Moreover, the maximum stress in cortical bone was sensitive to the quantity of integrated nodes at the bone margin: the lower the quantity, the higher the stress. Therefore, the optimization of the osseointegration pattern on the cortical bone/implant interface helped to increase the load-bearing capacity of the peri-implant bone and decrease the risk of overloading.
References 1. Pye AD, Lockhart DE, Dawson MP, et al: A review of dental implants and infection. J Hosp Infect 2009;72:104-110 2. Bidez MW, Misch CE: Issues in bone mechanics related to oral implants. Implant Dent 1992;1:289-294 3. Kitamura E, Stegaroiu R, Nomura S, et al: Biomechanical aspects of marginal bone resorption around osseointegrated implants: considerations based on a three-dimensional finite element analysis. Clin Oral Implants Res 2004;15: 401-412 4. Ruffoni D, Wirth AJ, Steiner JA, et al: The different contributions of cortical and trabecular bone to implant anchorage in a human vertebra. Bone 2012;50:733-738 5. Misch CE, Suzuki JB, Misch-Dietsh FM, et al: A positive correlation between occlusal trauma and peri-implant bone loss: literature support. Implant Dent 2005;14:108-116 6. Miyata T, Kobayashi Y, Araki H, et al: The influence of controlled occlusal overload on peri-implant tissue. Part 3: A histologic study in monkeys. Int J Oral Maxillofac Implants 2000;15:425-431 7. Miyata T, Kobayashi Y, Araki H, et al: The influence of controlled occlusal overload on peri-implant tissue: a histologic
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
9
Effect of Osseointegration Patterns on Bone Stress
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
10
Han et al
study in monkeys. Int J Oral Maxillofac Implants 1998;13:677-683 Isidor F: Loss of osseointegration caused by occlusal load of oral implants. A clinical and radiographic study in monkeys. Clin Oral Implants Res 1996;7:143-152 Ferrari DS, Piattelli A, Iezzi G, et al: Effect of lateral static load on immediately restored implants: histologic and radiographic evaluation in dogs. Clin Oral Implants Res 2015;26:e51-e56 Nagasawa M, Takano R, Maeda T, et al: Observation of the bone surrounding an overloaded implant in a novel rat model. Int J Oral Maxillofac Implants 2013;28:109-116 Tawil G: Peri-implant bone loss caused by occlusal overload: repair of the peri-implant defect following correction of the traumatic occlusion. A case report. Int J Oral Maxillofac Implants 2008;23:153-157 Quirynen M, Naert I, van Steenberghe D: Fixture design and overload influence marginal bone loss and fixture success in the Branemark system. Clin Oral Implants Res 1992;3:104-111 Pera P, Menini M, Bevilacqua M, et al: Factors affecting the outcome in the immediate loading rehabilitation of the maxilla: a 6-year prospective study. Int J Periodontics Restorative Dent 2014;34:657-665 Zweers J, van Doornik A, Hogendorf EA, et al: Clinical and radiographic evaluation of narrow- vs. regular-diameter dental implants: a 3-year follow-up. A retrospective study. Clin Oral Implants Res 2015;26:149-156 Baggi L, Cappelloni I, Di Girolamo M, et al: The influence of implant diameter and length on stress distribution of osseointegrated implants related to crestal bone geometry: a three-dimensional finite element analysis. J Prosthet Dent 2008;100:422-431 Huang HL, Chang CH, Hsu JT, et al: Comparison of implant body designs and threaded designs of dental implants: a 3-dimensional finite element analysis. Int J Oral Maxillofac Implants 2007;22:551-562 Yoon KH, Kim SG, Lee JH, et al: 3D finite element analysis of changes in stress levels and distributions for an osseointegrated implant after vertical bone loss. Implant Dent 2011;20:354-359 Pessoa RS, Muraru L, Junior EM, et al: Influence of implant connection type on the biomechanical environment of immediately placed implants-CT-based nonlinear, three-dimensional finite element analysis. Clin Implant Dent Relat Res 2010;12:219-234 Geng JP, Tan KB, Liu GR: Application of finite element analysis in implant dentistry: a review of the literature. J Prosthet Dent 2001;85:585-598 Lu J, Pan K, Xu X, et al: Influence of different bone contact ratio to stress distribution in bone around dental implant. J Oral Maxillofac Surg 2005;15:234-237 Han J, Hou J, Zhou G, et al: A histological and biomechanical study of bone stress and bone remodeling around immediately loaded implants. Sci China Life Sci 2014;57:618-626 Papavasiliou G, Kamposiora P, Bayne SC, et al: 3D-FEA of osseointegration percentages and patterns on implant-bone interfacial stresses. J Dent 1997;25:485-491 Xing X, Liu B: The influence of osseointegration patterns on implant2bone interfacial stresses. J Ch Med Univ 2002;23:152-154
24. Anitua E, Tapia R, Luzuriaga F, et al: Influence of implant length, diameter, and geometry on stress distribution: a finite element analysis. Int J Periodontics Restorative Dent 2010;30: 89-95 25. Yang J, Xiang HJ: A three-dimensional finite element study on the biomechanical behavior of an FGBM dental implant in surrounding bone. J Biomech 2007;40:2377-2385 26. Chang CL, Chen CS, Hsu ML: Biomechanical effect of platform switching in implant dentistry: a three-dimensional finite element analysis. Int J Oral Maxillofac Implants 2010;25:295-304 27. Lewinstein I, Banks-Sills L, Eliasi R: Finite element analysis of a new system (IL) for supporting an implant-retained cantilever prosthesis. Int J Oral Maxillofac Implants 1995; 10:355-366 28. Castano MC, Zapata U, Pedroza A, et al: Creation of a three-dimensional model of the mandible and the TMJ in vivo by means of the finite element method. Int J Comput Dent 2002;5:87-99 29. Sun Y, Kong L, Hu K, et al: Selection of the implant transgingival height for optimal biomechanical properties: a three-dimensional finite element analysis. Br J Oral Maxillofac Surg 2009;47:393-398 30. Kitamura E, Stegaroiu R, Nomura S, et al: Influence of marginal bone resorption on stress around an implant—a three-dimensional finite element analysis. J Oral Rehabil 2005;32:279-286 31. Okumura N, Stegaroiu R, Kitamura E, et al: Influence of maxillary cortical bone thickness, implant design and implant diameter on stress around implants: a three-dimensional finite element analysis. J Prosthodont Res 2010;54:133-142 32. Rancourt D, Shirazi, Adl A, et al: Friction properties of the interface between porous-surfaced metals and tibial cancellous bone. J Biomed Mater Res 1990;24:1503-1519 33. Sevimay M, Turhan F, Kilicarslan MA, et al: Three-dimensional finite element analysis of the effect of different bone quality on stress distribution in an implant-supported crown. J Prosthet Dent 2005;93:227-234 34. Mouhyi J, Dohan Ehrenfest DM, Albrektsson T: The periimplantitis: implant surfaces, microstructure, and physicochemical aspects. Clin Implant Dent Relat Res 2012;14:170-183 35. Lee C, Lin S, Kang M, et al: Effects of implant threads on the contact area and stress distribution of marginal bone. J Dent Sci 2010;5:156-165 36. Chang CL, Chen CS, Huang CH, et al: Finite element analysis of the dental implant using a topology optimization method. Med Eng Phys 2012;34:999-1008 37. van Staden RC, Guan H, Johnson NW, et al: Step-wise analysis of the dental implant insertion process using the finite element technique. Clin Oral Implants Res 2008;19:303-313 38. Graf H, Grassel H, Aeberhard H: A method for the measurement of occlusal forces in three directions. Helv Odont Scand 1974;18:7-11 39. Esposito M, Grusovin MG, Willings M, et al: The effectiveness of immediate, early, and conventional loading of dental implants: a Cochrane systematic review of randomized controlled clinical trials. Int J Oral Maxillofac Implants 2007;22:893-904
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
Key Lab for Biomechanics and Mechanobiology of Education Ministry, School of Biological and Medical Engineering, Beihang University, Beijing, China 2 Peking University School and Hospital of Stomatology, Beijing, China
Keywords Dental implant; finite element analysis; bone resorption; osseointegration; biomechanics. Correspondence Jingyun Han, Beihang University, XueYuan Road No. 37, HaiDian District, Beijing, China 100191. E-mail: [email protected] This study was supported by the National Natural Science Foundation of China (10902010 and 61227902). The authors deny any conflicts of interest. Accepted October 21, 2015 doi: 10.1111/jopr.12434
Abstract Purpose: To investigate the biomechanical performance of different osseointegration patterns between cortical bone and implants using finite element analysis. Materials and Methods: Fifteen finite element models were constructed of the mandibular fixed prosthesis supported by implants. Masticatory loads (200 N axial, 100 N oblique, 40 N horizontal) were applied. The cortical bone/implant interface was divided equally into four layers: upper, upper-middle, lower-middle, and lower. The bone stress and implant displacement were calculated for 5 degrees of uniform integration (0, 20%, 40%, 60%, and 100%) and 10 integration patterns. Results: The stress was concentrated in the bone margin and gradually decreased as osseointegration progressed, when the integrated and nonintegrated areas were alternated on the bone-implant surface. Compared with full integration, the integration of only the lower-middle layer or lower half layers significantly decreased von Mises, tensile, and compressive stresses in cortical bone under oblique and horizontal loads, and these patterns did not induce higher stress in the cancellous bone. For the integration of only the upper or upper-middle layer, stress in the cortical and cancellous bones significantly increased and was considerably higher than in the case of nonintegration. In addition, the maximum stress in the cortical bone was sensitive to the quantity of integrated nodes at the bone margin; lower quantity was associated with higher stress. There was no significant difference in the displacement of implants among 15 models. Conclusions: Integration patterns of cortical bone significantly affect stress distribution in peri-implant bone. The integration of only the lower-middle or lower half layers helps to increase the load-bearing capacity of peri-implant bone and decrease the risk of overloading, while upper integration may further increase the risk of bone resorption.
The introduction of osseointegrated implants symbolizes a turning point in clinical dental practice.1 Due to several advantages, such as being strong, durable, and natural in appearance, dental implants are often considered to be a more appealing option than conventional prostheses. However, preventing marginal bone loss around implants remains a significant challenge. Compared with natural teeth, implants have a lack of periodontal membrane support. The rigid connection with the alveolar bone is harmful to force dispersion. Moreover, cortical bone is about ten times stiffer than cancellous bone.2,3 As a result, cortical bone, although notably thin, plays a major role in the mechanical competence of implant anchorage.4 Excessive masticatory loads have been blamed for marginal bone loss around implants.5 Miyata et al6,7 observed three times
more bone loss when the controlled occlusal overload was produced by a superstructure in monkeys. Isidor8 and Ferrari et al9 reported breakdown of the crestal bone and the loss of osseointegration under nonaxial overloading in animal studies. Nagasawa et al10 established an implant occlusion model using rats, and revealed degenerative changes in osseointegration and/or in the peri-implant bone upon excessive loading. In addition, some clinical literature presents a positive correlation between high occlusal load and marginal bone loss.11,12 Pera et al13 and Zweerset al14 found that tapered implants and a wider implant diameter, which meant a decrease in bone stress15,16 , resulted in less marginal bone loss. Therefore, improving load transmission to decrease the stress level in marginal bone is a critical problem for osseointegrated implants.
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
1
Effect of Osseointegration Patterns on Bone Stress
Han et al
Figure 1 Cross-sectional view of FE models: (A) mandible segment with a dental implant and crown; (B) distribution of integrated layers.
Table 1 Material properties of the implant, crown, and cancellous bone Material Ti-6Al-4V implants Gold alloy crown Cancellous bone
Young’s modulus (MPa)
Poisson’s ratio
110,000 90,000 3000
0.35 0.3 0.3
Finite element (FE) analysis (FEA) has been an effective tool for studying the biomechanical problem of implantation.17-19 The quality of the bone/implant interface, such as integration percentage and patterns, may greatly affect stress distribution in peri-implant bone. Han et al and Lu et al constructed 3D FE models of implants, and concluded that the bone stress gradually decreased as osseointegration progressed.20,21 Papavasiliou et al and Xing and Liu designed five types of osseointegration patterns (locally alternating, coronal only, apical only, facial only, and lingual only) on the bone/implant interface at 50% osseointegration. Results showed that coronal integration decreased both crestal and apical stress, while the apical pattern induced higher apical stress.22,23 Additionally, regardless of osseointegration quality, implant shapes, and loading angle, a general rule in stress distribution emerges: cortical bone bears most of the masticatory load, and stress concentration occurs in the cortical bone margin.24,25 Accordingly, we proposed that changing osseointegration patterns, specifically on the cortical bone interface as opposed to the whole bone/implant interface, may be more favorable for homogeneous stress distribution and a lower stress magnitude. The purpose of this study is to develop 3D FE models of the single mandibular fixed prosthesis supported by implants and to evaluate the biomechanical performance of the different osseointegration patterns on the cortical bone/implant interface. Thus, these results may provide the theoretical basis for optimizing implant design and decreasing the risk of overloadinduced bone resorption.
Materials and methods The FE models consisted of four parts: cortical bone, cancellous bone, implant, and crown (Fig 1). A bone block ofthe mandible in the second premolar region was constructed based on the CT 2
image of an adult male patient. The cortical bone had a thickness of approximately 2 mm. Based on reverse engineering, a 4.1*12 mm screw-type dental implant and crown were reconstructed in commercial CAD software (Geomagic Studio, v8.0, Raindrop; Geomagic, Inc., Morrisville, NC) and I-DEAS (v.10.0, EDS, Plano, TX). All geometric models were meshed with 10-node tetrahedron elements. For sufficient accuracy in each case, a convergence test was performed to determine the number of elements. The convergence rate was less than 1% for stress and less than 0.5% for displacement. In total, the models consisted of 69,388 elements and 111,901 nodes. The material properties of implants, crown, and cancellous bone were assumed to be isotropic, homogeneous, and linearly elastic (Table 1).26,27 The cortical bone was represented by the anisotropic material model (Ex = 17 GPa, Ey = 13.8 GPa, Ez = 10.6 GPa; Gxy = 6.2 GPa, Gyz = 4.1 GPa, Gxz = 5.4 GPa; vxy = 0.38, vyz = 0.23, vxz = 0.47).28 Masticatory forces of 200 N, 100 N, and 40 N were applied to the center of the crown axially (AX), buccolingually (BL), and horizontally (HZ), respectively.29-31 The mesial and distal surfaces of the mandibular bone were constrained in x, y, and z directions (displacements = 0). Two contact types, “frictional contact” and “bonded contact,” were defined on the bone/implant interface. “Frictional contact” indicated a nonintegrated state and enabled frictional sliding (frictional coefficient, µ = 0.3).32 “Bonded contact” meant an integrated state, and there was no relative sliding and separation between implants and bone. In this study, the cancellous bone/implant interface was assumed to be bonded together perfectly. For the cortical bone, the different integration patterns were considered to simulate the following case. Model case 1: localized integration patterns (LIP)
The cortical bone/implant interface was divided equally into four layers along an axial direction: upper, upper-middle, lower-middle, and lower (Fig 1B).The localized integration patterns with different osseointegration percentages (OIP) were designed on the cortical bone/implant interface (Table 2). In the first type of model, only one of the four layers was
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
Han et al
Effect of Osseointegration Patterns on Bone Stress
Table 2 Model names with different integrated patterns Models
Region of localized integration
UIP
LIP 40-I LIP 40-II LIP 40-III LIP 40-IV LIP 60-V LIP 60-VI LIP 20-I LIP 20-II LIP 20-III LIP 20-IV
Upper layer Upper-middle layer Lower-middle layer Lower layer Upper and upper-middle layers Lower-middle and lower layers Upper layer Upper-middle layer Lower-middle layer Lower layer
40% 40% 40% 40% 60% 60% 20% 20% 20% 20%
60%. In the third type, only one of the four layers was designed as the integrated area, and the quantity of the bonded nodes was decreased by half. The total OIP was approximately 20% on the cortical bone/implant interface. In this study, the different models were named according to a combination of pattern types, OIP, and integrated layer (Table 2). The model of full osseointegration (OIP 100%) was the control, and a comparative analysis was performed to evaluate the effect of LIP on bone stress and implant displacement.
Model case 2: uniform integration patterns (UIP)
designated as the integrated area, while the other layers were the nonintegrated areas. The total OIP was approximately 40% on the cortical bone/implant interface. In the second type, only the upper half or only the lower half interfaces were defined as the bonded contacts, and the total OIP was approximately
UIP was used to simulate random osseointegration in cortical bone. The integrated and nonintegrated areas alternated on the cortical bone/implant interface. Five FE models with different OIPs (100%, 60%, 40%, 20%, 0) were constructed. For the UIP, a comparative analysis was performed to evaluate the effect of OIP on bone stress and implant displacement.
Figure 2 Von Mises stress distribution of the cortical bone in the LIP models with 40% OIP: (A) axial loading, (B) buccolingual loading, (C) horizontal loading.
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
3
Effect of Osseointegration Patterns on Bone Stress
Han et al
Figure 3 Von Mises stress at the cortical bone margin in the LIP models with 40% OIP: (A) axial loading, (B) buccolingual loading, (C) horizontal loadingand, (D) path.
Results
Table 3 Maximum von Mises stress in cortical and cancellous bone (MPa)
Von Mises stress in the cortical bone
In the LIP models with an OIP of 40%, the von Mises stress distribution in the cortical bone is shown in Figure 2. A similar stress concentration was observed in the models of LIP 40-I and LIP 40-II compared with the model of OIP 100%, and the maximum stresses were located in the cortical bone margin. By contrast, the stress distribution was more uniform in the LIP 40-III and LIP 40-IV models, and the starting position of bonded contact became another high stress region in addition to the cortical bone margin. The maximum stresses occurred in the LIP 40-I model. Under axial loading, a marked decrease in cortical bone stress was found, as the integrated region was transferred from layer I to IV. The maximum bone stress was reduced by up to 36.3% in the LIP 40-IV model as compared with the OIP 100% model. Under buccolingual and horizontal loading, the bone stress in the LIP 40-III model was lowest, and decreased by 24.9% and 16.6%, respectively (Fig 3). When OIP decreased to 20% in the LIP models, the highest stress in the cortical bone was located at the starting position of bonded contact. The stress contour plots (Fig 4) showed that the lower the integrated location, the more uniform the bone distribution; however, the LIP of OIP 20% did not improve the stress in the cortical bone, and even engendered higher stress. For example, the stress in the LIP 20-IV model was lowest, and the maximum stress increased by 29.0% to 61.2%, respectively, under buccolingual and horizontal load compared with that in
4
Models
UIP 20% UIP 40% UIP 60% OIP 100%
AX
BL Cortical bone
HZ
44.3 37.9 38.7 39.9
226.3 211.6 200.2 109.0
108.1 76.9 79.0 41.3
Cancellous bone LIP 40-IV LIP 20-III LIP 20-IV UIP 20% OIP 100%
10.38 10.38 10.47 10.59 10.21
23.61 23.16 26.71 22.03 17.45
11.21 11.02 12.72 10.41 8.87
the OIP 100% model. In addition, when OIP increased to 60% in the LIP models, LIP 60-V and LIP 60-VI were similar to OIP 100 and LIP 40-III, respectively, in stress distribution and magnitude. In the UIP models, the maximum stresses were located in the cortical bone margin. The bone stress gradually decreased (Table 3) as OIP increased. Under the same conditions of the OIP, bone stress in the UIP models was significantly higher than in the LIP models.
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
Han et al
Effect of Osseointegration Patterns on Bone Stress
Figure 4 Von Mises stress distribution of the cortical bone in the LIP models with 20% OIP: (A) axial loading, (B) buccolingual loading, (C) horizontal loading.
Von Mises stress in cancellous bone
The bone stress distribution was highly similar in all models. The stress concentration primarily occurred in the following areas:
r r r
The lingual side adjacent to the cortical bone, the first and last threads, and the apical area under AX The top adjacent to the cortical bone and the first threads under BL The lingual side adjacent to the cortical bone and the first threads under HZ
Under AX, a slight change in stress was observed in all models. Under BL and HZ, stress significantly increased in the LIP 40-IV, LIP 20-III, LIP 20-IV, and UIP 20% models compared with the OIP 100% model (Fig 5, Table 3). The biggest difference occurred in the LIP 20-IV model, and the
maximum stress increased by 53.2% and 36.6%, respectively, under BL and HZ. Principal stress in peri-implant bone
In the LIP models with OIP at 40%, the principal stress distribution in the cortical bone is shown in Figure 6 and 7. The stress concentration occurred at the start site of bonded contact. Compared with the OIP 100% model, the LIP models increased the maximum principal stress under AX (Table 4), but the maximum principal stress under BL and HZ and the minimum principal stress significantly decreased in the LIP 40-III and LIP 40-IV models. In cancellous bone, the stress concentration was located at the top side adjacent to the cortical bone, the first threads, and the apical area. Under AX, there was no significant difference in principle bone stress between the full integrated model and
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
5
Effect of Osseointegration Patterns on Bone Stress
Han et al
Figure 5 Von Mises stress distribution in the cancellous bone: (A) axial loading, (B) buccolingual loading, (C) horizontal loading.
the LIP models with OIP at 40% (Table 4). On the contrary, the principal stress gradually increased as the bonded contact moved to the lower position under BL and HL. The biggest difference in stress was observed in the LIP 40-IV model, and 6
the maximum tensile and compressive stress increased approximately two times and 48.8%, respectively. In addition, the LIP models with OIP at 20% were similar to the models of LIP with OIP at 40% in bone stress
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
Han et al
Effect of Osseointegration Patterns on Bone Stress
Table 4 Maximum tensile and compressive stress in cortical and cancellous bone (MPa) AX
OIP 100% LIP 40-Ⅰ LIP 40-Ⅱ LIP 40-Ⅲ LIP 40-Ⅳ
+9.9/–58.4 +20.0/–61.9 +37.9/–37.8 +33.7/–31.6 +37.9/–29.7
BL Cortical bone
HO
+153.8/–155.2 +164.5/–163.2 +124.1/–100.7 +88.5/–90.1 +84.9/–91.6
+61.0/–67.9 +65.8/–71.4 +46.6/–42.2 +39.2/–38.1 +52.1/–38.9
Cancellous bone OIP 100% LIP 40-Ⅰ LIP 40-Ⅱ LIP 40-Ⅲ LIP 40-Ⅳ
+12.5/–12.4 +12.9/–12.7 +12.8/–12.8 +12.9/–13.1 +13.2/–13.6
+6.2/–6.4 +6.7/–6.7 +8.2/–7.5 +10.3/–8.6 +12.8/–10.4
+3.5/–4.1 +3.9/–4.6 +4.7/–4.6 +5.8/–5.3 +7.2/–6.1
Table 5 Maximum implant displacement (µm)
OIP 100% LIP 40-I LIP 40-II LIP 40-III LIP 40-IV LIP 20-I LIP 20-II LIP 20-III LIP 20-IV LIP 60-V LIP 60-VI
AX
BL
HO
6.26 6.28 6.35 6.76 6.85 6.37 6.40 6.49 6.56 6.27 6.43
16.48 16.62 17.25 18.26 19.34 17.63 18.13 19.11 19.99 16.49 18.24
10.12 10.21 10.53 11.09 11.68 10.76 11.03 11.56 12.04 10.13 11.02
distribution, but there was higher stress in the peri-implant bone under BL and HL in the LIP models with OIP at 20%. The models of LIP 60-V and LIP 60-VI were similar to OIP 100% and LIP 40-III, respectively, in stress distribution and magnitude. Displacement of implants
The maximum displacement occurred on the implant neck adjacent to the bone margin. There was a slight difference between the full integrated model and the LIP models (Table 5). It was determined that a lower osseointegration location and OIP could induce higher displacement of implants. Accordingly, the maximum displacement was observed in the LIP 20-IV model.
Discussion Stress concentration in marginal bone has been suggested to be a direct cause of bone resorption and osseointegration failure.15,33 Many studies have tried to optimize implant material properties, implant structure, and surgical procedures to regulate stress levels in the peri-implant bone.24,25,34,35 In the present study, we were more concerned with the biomechanical performance of the cortical bone/implant interface and hypothesized that the
LIP can significantly affect stress distribution in the cortical bone. Accordingly, we developed fifteen 3D FE models with different integrated patterns. In the LIP models with OIP at 40%, the FE results showed that the osseointegration patterns on the cortical bone/implant interface significantly affected the von Mises stress distribution and magnitude in the cortical bone. The bone stress at the start of the bonded contact gradually became comparable to that at the bone margin, as the bonded contact moved to the lower position on the interface of the cortical bone. This meant that the masticatory force was more uniformly transmitted to the cortical bone. As a consequence, the bone stress magnitude significantly decreased compared with that in the model with OIP at 100%, where the integration of only the lower-middle layer or lower half interface occurred. Additionally, principle stress was calculated in the present study.36 We found that the patterns of LIP 40-III and LIP 40-IV could remarkably decrease compressive and tensile stress in cortical bone under BL and HL, and bone tensile stress in the LIP models increased under AX. It is generally known that an oblique and horizontal load is more dangerous than an axial load clinically. The results in this study showed that the bone stress induced by AX was far lower than that induced by BL and HZ, and the data substantiated clinical experience. Overall, the patterns that occurred on only the lower-middle, lower layer, or lower half interface helped to prevent the marginal bone from overloading. To evaluate the effect of osseointegration patterns more comprehensively, models of UIP and LIP with different OIPs were developed. The results showed that the integrated state of the bone margin was a key factor affecting stress level in the cortical bone. When the bone margin completely integrated with the implant, there was no significant difference in cortical bone stress between the full integration and the LIP (e.g., OIP 100% vs. LIP 60-I and OIP 100% vs. LIP 40-I), though the integrated area in the LIP models was lower than in the OIP 100% model. On the contrary, when integration of the bone margin did not occur, the starting position of bonded contact and the number of integrated nodes at the starting position could significantly affect the stress level in the cortical bone. We observed that both conditions were conducive to uniform stress distribution: (1) the starting position of the osseointegration was no higher than the lower-middle layer; and (2) nodes at the starting position were fully integrated. Therefore, the models of LIP 40-III, LIP 60VI, and LIP 40-IV showed better biomechanical performance than the model of full integration. These results reveal that optimization of integration patterns on the cortical bone/implant interface may help improve bone stress distribution more than simply increasing OIP between the bone and implants. Moreover, low OIP at the cortical bone margin would increase the overloading risk of the peri-implant bone. Stress in the cancellous bone has also been of concern in the present study. The results showed that von Mises stress increased when localized integration occurred on the lower layer or when the OIP was very low. In addition, the results showed that principle stress gradually increased as the starting position of localized integration moved to the lower layer. Overall, although the stress in the cancellous bone increased in some LIP models compared with the model of full integration, the largest difference was less than 7.0 MPa. Based on the above data, it
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
7
Effect of Osseointegration Patterns on Bone Stress
Han et al
Figure 6 Tensile stress distribution in the cortical bone: (A) axial loading, (B) buccolingual loading, (C) horizontal loading.
can be observed that stress in cancellous bone is not only far lower than stress in the cortical bone but also far lower than the yield stress of the cancellous bone (53 MPa).37 By contrast, stress in cortical bone has exceeded the yield stress of cortical bone in some models. Accordingly, the results indicate that the risk of overloading in cortical bone is apparently higher than in cancellous bone. Rigid fixation of implants is one of the evaluation criteria for a successful dental implant. Healthy implants should move less than 75 µm during chewing,36 and failure of dental implants could occur if the movement of implants is more than 500 µm. In the present study, the osseointegration patterns affected the displacement of implants, but the maximum difference was less than 4.3 µm between the model of full integration and LIP models. Moreover, the displacement of implants was far lower than 75 µm in all models. Therefore, from a mechanical viewpoint, the osseointegration patterns of the cortical bone/implant interface cannot significantly affect the stability of implants. For the FEA of dental implants, it is important to consider not only axial and horizontal forces but also a combined load
8
(oblique force), because the latter represents a more realistic occlusal direction. Generally, AX is much higher than BL and HZ. Graf et al38 found a ratio of 5:2.5:1 during chewing, and this ratio was used in the present study. Furthermore, it is well known that BL and HZ cause higher torque than AX. Our FE results showed that bone stress under BL and HZ was significantly higher than under AX, especially in the UIP models. Therefore, the results indicate that the case analyses for oblique and horizontal loading should not be ignored in FE models of dental implants, using occlusal adjustment to reduce the oblique or horizontal forces on the premise of a normal occluding relation is recommended for crown design. In the present study, we supported our hypothesis using the FE method, and the results will be verified through a comparison with experimental data in future studies. Additionally, immediate loading has been a more attractive treatment method in the clinic than delayed loading.39 The material property of peri-implant bone varies from soft connective tissue to complete bone maturation during the osseointegration process. The effects of different osseointegration patterns on bone stress are
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
Han et al
Effect of Osseointegration Patterns on Bone Stress
Figure 7 Compressive stress distribution in the cancellous bone (A) axial loading, (B) buccolingual loading, and (C) horizontal loading.
still unclear during different integration phases. Accordingly, this topic will be researched in our future work.
Conclusion Under functional forces, high stress is primarily located in the marginal bone around implants. The osseointegration patterns on the cortical bone/implant interface can significantly affect stress distribution and magnitude in the cortical bone. Compared with full integration, the integrated patterns that occurred only on the lower-middle layer or lower half interface can induce lower von Mises stress, and can significantly decrease compressive and tensile stress in the cortical bone under BL and HL. Moreover, the maximum stress in cortical bone was sensitive to the quantity of integrated nodes at the bone margin: the lower the quantity, the higher the stress. Therefore, the optimization of the osseointegration pattern on the cortical bone/implant interface helped to increase the load-bearing capacity of the peri-implant bone and decrease the risk of overloading.
References 1. Pye AD, Lockhart DE, Dawson MP, et al: A review of dental implants and infection. J Hosp Infect 2009;72:104-110 2. Bidez MW, Misch CE: Issues in bone mechanics related to oral implants. Implant Dent 1992;1:289-294 3. Kitamura E, Stegaroiu R, Nomura S, et al: Biomechanical aspects of marginal bone resorption around osseointegrated implants: considerations based on a three-dimensional finite element analysis. Clin Oral Implants Res 2004;15: 401-412 4. Ruffoni D, Wirth AJ, Steiner JA, et al: The different contributions of cortical and trabecular bone to implant anchorage in a human vertebra. Bone 2012;50:733-738 5. Misch CE, Suzuki JB, Misch-Dietsh FM, et al: A positive correlation between occlusal trauma and peri-implant bone loss: literature support. Implant Dent 2005;14:108-116 6. Miyata T, Kobayashi Y, Araki H, et al: The influence of controlled occlusal overload on peri-implant tissue. Part 3: A histologic study in monkeys. Int J Oral Maxillofac Implants 2000;15:425-431 7. Miyata T, Kobayashi Y, Araki H, et al: The influence of controlled occlusal overload on peri-implant tissue: a histologic
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
9
Effect of Osseointegration Patterns on Bone Stress
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
10
Han et al
study in monkeys. Int J Oral Maxillofac Implants 1998;13:677-683 Isidor F: Loss of osseointegration caused by occlusal load of oral implants. A clinical and radiographic study in monkeys. Clin Oral Implants Res 1996;7:143-152 Ferrari DS, Piattelli A, Iezzi G, et al: Effect of lateral static load on immediately restored implants: histologic and radiographic evaluation in dogs. Clin Oral Implants Res 2015;26:e51-e56 Nagasawa M, Takano R, Maeda T, et al: Observation of the bone surrounding an overloaded implant in a novel rat model. Int J Oral Maxillofac Implants 2013;28:109-116 Tawil G: Peri-implant bone loss caused by occlusal overload: repair of the peri-implant defect following correction of the traumatic occlusion. A case report. Int J Oral Maxillofac Implants 2008;23:153-157 Quirynen M, Naert I, van Steenberghe D: Fixture design and overload influence marginal bone loss and fixture success in the Branemark system. Clin Oral Implants Res 1992;3:104-111 Pera P, Menini M, Bevilacqua M, et al: Factors affecting the outcome in the immediate loading rehabilitation of the maxilla: a 6-year prospective study. Int J Periodontics Restorative Dent 2014;34:657-665 Zweers J, van Doornik A, Hogendorf EA, et al: Clinical and radiographic evaluation of narrow- vs. regular-diameter dental implants: a 3-year follow-up. A retrospective study. Clin Oral Implants Res 2015;26:149-156 Baggi L, Cappelloni I, Di Girolamo M, et al: The influence of implant diameter and length on stress distribution of osseointegrated implants related to crestal bone geometry: a three-dimensional finite element analysis. J Prosthet Dent 2008;100:422-431 Huang HL, Chang CH, Hsu JT, et al: Comparison of implant body designs and threaded designs of dental implants: a 3-dimensional finite element analysis. Int J Oral Maxillofac Implants 2007;22:551-562 Yoon KH, Kim SG, Lee JH, et al: 3D finite element analysis of changes in stress levels and distributions for an osseointegrated implant after vertical bone loss. Implant Dent 2011;20:354-359 Pessoa RS, Muraru L, Junior EM, et al: Influence of implant connection type on the biomechanical environment of immediately placed implants-CT-based nonlinear, three-dimensional finite element analysis. Clin Implant Dent Relat Res 2010;12:219-234 Geng JP, Tan KB, Liu GR: Application of finite element analysis in implant dentistry: a review of the literature. J Prosthet Dent 2001;85:585-598 Lu J, Pan K, Xu X, et al: Influence of different bone contact ratio to stress distribution in bone around dental implant. J Oral Maxillofac Surg 2005;15:234-237 Han J, Hou J, Zhou G, et al: A histological and biomechanical study of bone stress and bone remodeling around immediately loaded implants. Sci China Life Sci 2014;57:618-626 Papavasiliou G, Kamposiora P, Bayne SC, et al: 3D-FEA of osseointegration percentages and patterns on implant-bone interfacial stresses. J Dent 1997;25:485-491 Xing X, Liu B: The influence of osseointegration patterns on implant2bone interfacial stresses. J Ch Med Univ 2002;23:152-154
24. Anitua E, Tapia R, Luzuriaga F, et al: Influence of implant length, diameter, and geometry on stress distribution: a finite element analysis. Int J Periodontics Restorative Dent 2010;30: 89-95 25. Yang J, Xiang HJ: A three-dimensional finite element study on the biomechanical behavior of an FGBM dental implant in surrounding bone. J Biomech 2007;40:2377-2385 26. Chang CL, Chen CS, Hsu ML: Biomechanical effect of platform switching in implant dentistry: a three-dimensional finite element analysis. Int J Oral Maxillofac Implants 2010;25:295-304 27. Lewinstein I, Banks-Sills L, Eliasi R: Finite element analysis of a new system (IL) for supporting an implant-retained cantilever prosthesis. Int J Oral Maxillofac Implants 1995; 10:355-366 28. Castano MC, Zapata U, Pedroza A, et al: Creation of a three-dimensional model of the mandible and the TMJ in vivo by means of the finite element method. Int J Comput Dent 2002;5:87-99 29. Sun Y, Kong L, Hu K, et al: Selection of the implant transgingival height for optimal biomechanical properties: a three-dimensional finite element analysis. Br J Oral Maxillofac Surg 2009;47:393-398 30. Kitamura E, Stegaroiu R, Nomura S, et al: Influence of marginal bone resorption on stress around an implant—a three-dimensional finite element analysis. J Oral Rehabil 2005;32:279-286 31. Okumura N, Stegaroiu R, Kitamura E, et al: Influence of maxillary cortical bone thickness, implant design and implant diameter on stress around implants: a three-dimensional finite element analysis. J Prosthodont Res 2010;54:133-142 32. Rancourt D, Shirazi, Adl A, et al: Friction properties of the interface between porous-surfaced metals and tibial cancellous bone. J Biomed Mater Res 1990;24:1503-1519 33. Sevimay M, Turhan F, Kilicarslan MA, et al: Three-dimensional finite element analysis of the effect of different bone quality on stress distribution in an implant-supported crown. J Prosthet Dent 2005;93:227-234 34. Mouhyi J, Dohan Ehrenfest DM, Albrektsson T: The periimplantitis: implant surfaces, microstructure, and physicochemical aspects. Clin Implant Dent Relat Res 2012;14:170-183 35. Lee C, Lin S, Kang M, et al: Effects of implant threads on the contact area and stress distribution of marginal bone. J Dent Sci 2010;5:156-165 36. Chang CL, Chen CS, Huang CH, et al: Finite element analysis of the dental implant using a topology optimization method. Med Eng Phys 2012;34:999-1008 37. van Staden RC, Guan H, Johnson NW, et al: Step-wise analysis of the dental implant insertion process using the finite element technique. Clin Oral Implants Res 2008;19:303-313 38. Graf H, Grassel H, Aeberhard H: A method for the measurement of occlusal forces in three directions. Helv Odont Scand 1974;18:7-11 39. Esposito M, Grusovin MG, Willings M, et al: The effectiveness of immediate, early, and conventional loading of dental implants: a Cochrane systematic review of randomized controlled clinical trials. Int J Oral Maxillofac Implants 2007;22:893-904
C 2016 by the American College of Prosthodontists Journal of Prosthodontics 00 (2016) 1–10
