Functional Assessment of Dental Implant Osseointegration

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Po-Chun Chang, DDS, PhD* The aim of dental implant treatment William V. Giannobile, DDS, DMSc** is to restore function and esthetics within acceptable biocompatibil- ity. Formation of a direct structural and functional connection between the implant and supporting tis- Functional ankylosis of dental implants in alveolar bone is the current criterion sues, termed osseointegration, has to assess implant osseointegration from a biomechanical standpoint. In this emerged as the criterion used to literature review, the clinical significance and current available assessments evaluate long-term success.1 Much of implant stability are discussed. However, these assessments demonstrate effort has been devoted to facili- a variety of correlations to peri-implant structures and as such are difficult tating osseointegration, including to translate to the clinical arena. Calculating the effective stiffness from the improvement of surgical proce- homogenization of peri-implant tissues appears to be a more reliable approach dures and postsurgical care, devel- to predict implant stability in preclinical studies, but the structure-biomechanical relationship remains a clinical challenge. Despite the limitations in functional oping favorable implant geometry assessments of dental implant stability and oral implant biomechanics, this and surface properties, and incor- review highlights some emerging approaches to adapt these measures to porating bioactive factors (Table 1).2 clinical situations. (Int J Periodontics Restorative Dent 2012;23:e147–e153.) Osseointegration is a dynamic process that involves mechanical and biologic fixation.11 Upon insertion, the implant is immediately secured in the host bone by mechanical interlocking (primary implant stability). Subsequently, *Assistant Professor, Discipline of Periodontics, Faculty of Dentistry, National University of the biologic remodeling process Singapore, Singapore, Singapore. occurring at the tissue-implant in- **Professor, Department of Periodontics and Oral Medicine, School of Dentistry; Professor, Department of Biomedical Engineering, College of Engineering; and Director, Michigan terface determines the functional Center for Oral Health Research, School of Dentistry, University of Michigan, Ann Arbor, adaptation of implants (secondary Michigan, USA. implant stability).12 Peri-implant structure analyses and biomechani- Correspondence to: Po-Chun Chang, Faculty of Dentistry, National University of Singapore, 11 Lower Kent Ridge Road, Singapore 119083, Singapore; fax: +65-6773- cal examinations could be feasible 2602; email: [email protected]. approaches to evaluate the progres-

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Table 1 Factors affecting osseointegration

Factors Ways to evaluate Bone quality and quantity3 Histology, radiography, tactile perception Implant design4 Finite element analysis, biomechanical assessments Surgical technique5,6 Radiography, histology, biomechanical assessments, finite element analysis, perceptions from surgeon and patient Postsurgical care7,8 Radiography, histology, biomechanical assessments, local symptoms and signs, local biomarkers, perception from patient Bone modeling/remodeling9,10 Histology, radiography, local biomarkers Systemic health7 Hematology and clinical chemistry, radiography, physical examinations

sion of osseointegration.13 However, primary implant stability, including but the peri-implant structure was limitations still exist, and it remains atraumatic surgery to maintain the significantly destroyed, resulting of value to develop an effective mo- cellular viability and prevent tissue in difficulty translating the results dality to evaluate the dynamics of loss,15 greater final insertional torque to any area-independent property osseointegration for the purposes to ensure implant fixation,16 and a (Fig 1a).18 Applying a force parallel of diagnosis and prognosis of im- bone-condensing technique (eg, to the interface to push or pull out plant placement. The purposes of osteotome) to increase the area of the implant from host bone then this review were to summarize the bone-implant contact.17 appears to be feasible and possibly state of the art in assessing osseo- the most accessible approach to integration and provide a brief over- evaluate contact stiffness (Fig 1a).19 view of the scientific fundamentals Biomechanical assessments The applied load and implant dis- as well as the clinical significance of for preclinical investigations placement are recorded during osseointegration. the procedure, and the interfacial Implant stability relies on the con- failure (detaching of the implant) tact stiffness between the implant occurs with the maximum load ap- Clinical significance of and surrounding tissue, and a vari- plied. Interfacial stiffness is defined implant stability ety of biomechanical assessments as the slope of the tangent on the have been utilized for this purpose load-displacement curve before The initial stability of implants is (Table 2). the breakpoint.19 This method considered to be one of the prereq- An early attempt to evaluate causes minimal interfacial tissue uisites of implant success. Histologi- implant stability was the tensional damage for cylinder-type implants cally, the primarily unstable implant test, referring to the application of and is considered suitable for pre- prevents direct bone-implant contact a lateral force to detach titanium clinical proof-of-concept investiga- and results in fibrous tissue attach- plates or cylinders from the sup- tions.20 However, the disadvantage ment.14 Thus, several surgical tech- porting tissue.18 Implant stability of push-out tests is that the implant niques were suggested to improve was presented as lateral resistance, must be placed transcortically,

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which is only possible for cylinder osseointegration based on visual lize this metric in clinical dentistry. smooth-surfaced implants. The de- and acoustic observations. How- Nevertheless, it is believed that the structive nature provided limited ever, this methodology is relatively firm initial fixation of the implant information for fully osseointegrat- subjective and not sensitive to mi- facilitates the process of osseointe- ed or screw-type implants.20 nor changes over time.13 Damping gration and confers permanent im- Removal torque testing, in- characteristics, referring to tissue re- plant stability. However, at present, troduced by Roberts et al26 and covery after applying a signal, were the correlation between primary modified by Johansson and Al- recommended for implant stability and secondary implant stability still brektsson,27 measures the contact assessment.29 The Periotest (Med- cannot be confirmed scientifically.32 stiffness by unscrewing the implant. izinktechnik Gulden), originally de- The removal torque is equivalent signed to evaluate the stability of to the interfacial shear calibrated natural teeth based on electromag- Correlation between in Newton centimeters (Ncm) by netically driven forces, has been implant stability and the a torque manometer (Fig 1b). The used for the evaluation of implant peri-implant structure critical torque value occurs while stability since 1990 (Fig 1c).30 How- breaking the tissue interface. The ever, the limitation of the Periotest Alveolar bone provides major sup- main criticism of this method is that measurement is the narrow range port for dental implants and is con- implant surface specifications may permitted, leading to a lack of sidered to affect implant stability. significantly influence the results, sensitivity in osseointegration. This Early histologic and radiographic and the process is still destructive.2 limitation is presumably due to studies on human cadavers demon- the physical differences between strated a significant correlation be- the periodontium and implant- tween primary implant stability and Clinical implant stability supporting structure. The position cortical bone thickness.32 Three- assessments of the percussion rod may also in- dimensional computed tomogra- fluence the results.31 phy (CT) assessment revealed that The prerequisite for the clinical as- Resonance frequency analysis the radiographic density of bone sessment of implant stability is no (RFA) was also developed based may contribute to primary bone sta- destruction of the surrounding host on the damping characteristics of bility,22 and this relationship tended tissues. Thus, measurement during vibration, thereby overcoming the to be closer in a wider-dimensioned implant insertion was developed limitations of the Periotest by using implant.33 Interestingly, the CT to predict primary implant stabil- an L-shaped transducer to fix the measurement also demonstrated ity, including cutting resistance and position and allowing a wider range that greater trabecular thickness insertional torque. Both measure- of detection (Fig 1d).13 The contact and density of the cancellous bone ments consider the lateral com- stiffness is converted from the peak lead to stronger primary stabil- pression force and friction during of the frequency-amplitude plot, ity, whereas trabecular separation implant placement. Therefore, in- and a higher frequency as well as a might reduce the stability.23 direct measurement revealed some sharp peak indicates better implant The correlation between sec- correlation but also a discrepancy stability.2,13 However, damping is a ondary implant stability and the from the direct measurement of re- complex mechanical phenomenon, peri-implant structure has been removal torque, and the correlation and the reading value of RFA (the ported since the late 1990s when between cutting resistance and in- implant stability quotient) is not Johansson and colleagues ob- sertional torque is still unclear.28 a linear unit. The clinical value of served a similar trend in the histo- Percussion testing is a common RFA is still questionable. Further logic change between the bone clinically used method to evaluate studies are needed to better uti- in contact with the implant and

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Table 2 Biomechanical assessments of implant stability

Methodology Property investigated Parameters Primary stability Secondary stability Clinical use Destructive Precision Relevance to structure Tensional18 Lateral resistance Maximal lateral load Yes Yes No Yes ++ NA Push-/pull-out19,20 Interfacial shear Maximal force, interfacial stiffness Yes Yes No Yes ++ ++ Cutting resistance21 Bone quality Cutting energy Yes No Yes Yes ++ ++ Insertional torque22,23 Interfacial shear Torque load, peak insertional torque Yes No Yes No ++ ++ Removal torque24,25 Interfacial shear Torque load, loosening torque No Yes No Yes ++ ++ Periotest9 Ultrasonics/ damping Periotest value Yes Yes Yes No + + Resonance frequency analysis23 Vibration/ damping Implant stability quotient Yes Yes Yes No + + In vivo finite element optimization20 Effective tissue stiffness Functional apparent moduli NA Yes Yes No ++ ++

+ = method with mild/doubtful precision/relevance; ++ = method with definite precision/relevance; NA = relevance not determinable/has not been determined.

Electromechanical

Attached Direction Torque transducer of force

Gingiva Gingiva Gingiva Gingiva Connective Connective Connective Connective tissue tissue tissue tissue

Alveolar Alveolar Alveolar Alveolar bone bone bone bone

a b c d

Fig 1 Currently available biomechanical assessments of implant stability. (a) Tensional/pull-out/push-out test; (b) insertion/removal torque; (c) Periotest; and (d) resonance frequency analysis. Arrows indicate the direction of external load from the devices.

removal torque.24 Brånemark et moval torque. However, an implant development of nondestructive as- al25 demonstrated that both bone pulling out after unscrewing might sessment devices (Periotest, RFA), observed in contact with the im- still cause significant damage and researchers demonstrated that his- plant histologically and total bone influence the assessment of the tologic bone-implant contact and thickness were correlated with re- peri-implant structure. Given the bone density tended to correlate

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Table 2 Biomechanical assessments of implant stability

+ = method with mild/doubtful precision/relevance; ++ = method with definite precision/relevance; NA = relevance not determinable/has not been determined.

with the mechanical impedance.9,34 condition, and the result is usu- interfacial stiffness than any of the Recent preclinical studies using ally presented as the distribution individual structural parameters. micro-CT imaging indicated moder- of stress and strain in the model.2 FBAM and FCAM became consis- ate to strong correlations between FE models have been used to de- tent when reaching a certain tissue peri-implant structural parameters sign dental implants and implant- thickness, which was named as the and biomechanical assessments.10,20 supported prostheses, evaluate functionally relevant peri-implant However, information from CT im- the quality of supporting bone, layer. This layer may be regarded aging should be interpreted care- determine the implant treatment as a reference range for assessing fully because of the inability to plan, and predict the long-term the functional dynamic of dental eliminate radiographic artifacts.35 survival of implants.2 Bone-implant implant osseointegration. contact stiffness is usually considered as a predetermined variable, Finite element analysis and and the effective stiffness could Conclusions functional apparent moduli only be calculated via the homogenization of the peri-implant struc- Unfortunately, to date, there is Finite element (FE) analysis has ture (Fig 2).20 In a recent study, the still no ideal assessment that can been widely applied to the field functional bone apparent modulus translate directly to the level of of implant dentistry to assess bio- (FBAM, referring to the stiffness osseointegration, and a degree mechanical influences on the den- of the bone of interest) and func- of discrepancy still exists among tal implant and supporting tissue.2 tional composite tissue apparent assessments used to determine The analysis is based on a theoretic modulus (FCAM, referring to the dental implant stability. CT and model whereby the structure and stiffness of the entire tissue of inter- micro-CT imaging appears to pro- conditions are predetermined by est) were calculated,20 and it was vide comprehensive information, reference landmarks and assump- demonstrated that both FBAM and but radiographic artifacts on the tions based on the physiologic FCAM had stronger correlations to measurements can limit clinical

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Fig 2 Effective tissue stiffness calculated from in vivo FE optimization for application to implant stability. This figure demonstrates an example calculating the functional bone apparent modulus (one of the effective tissue stiffness, referring to the effective stiffness of the bone structure in this area) in a specific peri-implant zone. The peri-implant structural information is acquired from a three-dimensional micro-CT image (top panel). The position Microscopic model Optimizing model of the dental implant (yellow box in top panel) and range of peri-implant structure (blue box in top panel) are identified. The radiographic information is then transferred to establish FE models (middle panel). In the microscopic model, each element presents unique mechanical properties according to the radiographic density. In the optimizing model, the effective stiffness of bone tissue within the area of interest (deep yellow portion within the area bound by the red lines) is assumed homogenous and unknown. After applying an equivalent simulated load on both models, the strain distribution is recorded in both models (bottom panel). The simulated result within the area of interest (area bound by red lines in middle and bottom panels) in both models is approximated and optimized to calculate the effective stiffness (functional bone apparent modulus) of the bone structure within the area of interest.

Approximation

Effective stiffness (functional bone apparent modulus)

implementations. Nondestructive gration. These advances have Acknowledgments devices for biomechanical as- certainly improved understanding sessments are being developed, in the development of improved The authors would like to thank Benjamin Ng and Qi Qi Lee for their support with the but their precision and clinical surrogates for osseointegration and illustrations. This work was supported by the relevance still needs to be eluci- implant biomechanics; however, ITI Foundation, the AO Foundation, and dated. The effective stiffness from there remain significant challeng- NUS-MOE research grants. homogenizing the peri-implant es in the measurement of dental structures seems feasible to pres- implant stability in the structure- ent the dynamics of osseointe- biomechanical relationship.

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