- Email: [email protected]
Assessing bone's adaptive capacity around dental implants
COVER
STORY
Assessing bone’s adaptive capacity around dental implants A literature review Gary Greenstein, DDS, MS; John Cavallaro, DDS; Dennis Tarnow, DDS
D
ental implants are an integral facet of restorative therapy and have a high survival rate.1-3 However, researchers and clinicians are concerned that certain types or aspects of prosthetic restorations supported by dental implants (such as cantilevered prostheses, angulated abutments, prostheses with increased crown-to-implant ratios, implants connected to teeth) are associated with increased stress,4-6 which may reduce their survival rates. In this regard, the above prosthetic constructs have not demonstrated increased failure rates when compared with the rate of implant loss associated with prosthetic constructs that are not exposed to increased stress.7-10 With respect to prosthetic constructs that experience increased stress, several authors have provided clinical guidelines regarding ways to enhance clinical success.7-10 Therefore, it is important that clinicians be familiar with contemporary perspectives concerning the bone’s response to placement of dental implants. We review concepts pertaining to bone adaptation that 362 JADA 144(4)
http://jada.ada.org
AB STRACT Background. Increased stress (force) on prostheses induces strain (deformation) in the peri-implant bone. Elevated stress and strain could result in the failure of implants that support prostheses. However, the survival rate of implants supporting prostheses under increased stress is high. Either the bone is stronger than expected or it adapts to increased stress. Concepts regarding bone’s adaptive capacity continue to evolve and are the focus of this literature review. Types of Studies Reviewed. The authors searched the literature to find studies that addressed the bone’s capacity to adjust to increased stress and strain. They assessed experimental and clinical trials in which investigators monitored healing after placement of dental implants. Results. The data indicate that forces greater than the bone’s adaptive ability can induce loss of osseointegration, as well as osseous resorption. In contrast, it is possible that increased stress on prostheses initiates a reparative process, thereby facilitating retention of implants experiencing increased stress. Numerous lines of evidence support the concept that bone can modify itself to withstand increased mechanical forces. Practical Implications. The authors provide an explanation for the high success rate of prostheses and implants in bone that are exposed to increased stress and strain. Key Words. Bone; dental implants; osseointegration; resorption. JADA 2013;144(4):362-368. Dr. Greenstein is a clinical professor, Department of Periodontology, College of Dental Medicine, Columbia University, New York City, and is in private practice in Freehold, N.J. Address reprint requests to Dr. Greenstein, 900 W. Main St., Freehold, N.J. 07728, e-mail [email protected]. Dr. Cavallaro is an associate clinical professor, Department of Prosthodontics, and director, Implant Fellowship Program, College of Dental Medicine, Columbia University, New York City, and is in private practice in Brooklyn, N.Y. Dr. Tarnow is director of dental implant education and a clinical professor, Department of Periodontology, College of Dental Medicine, Columbia University, New York City, and is in private practice in New York City.
April 2013
Copyright © 2013 American Dental Association. All Rights Reserved.
COVER
may account for high survival rates of prostheses that are subjected to increased stresses. Bone Mechanotransduction
Bone mechanotransduction is the mechanism that permits bone to detect stimuli, but this process is not understood completely. It is thought that bone cells sense and respond to their mechanical environment by changing their biological and biochemical actions.11 We need to underscore that it is the strain (deformation or elongation in response to stress), not stress (force acting on bone), that precipitates alteration of the bone’s response.11 In this regard, stress and strain concentrations are affected by bone quality; dense bone is more resistant to deformation than is less dense bone.12 In addition, other factors can affect the strain response, such as the bone-implant interface and bone elasticity.13 Osteocytes are thought to respond to one of three possible stimuli: direct mechanical stimulation, fluid flow induced by shear stress or bone microdamage.14 The prevailing concept suggests that under dynamic loading, bone matrix deformation produces an interstitial fluid flow in the lacunocanalicular system.14 This fluid creates shear stress that stimulates osteocytes. Osteocytes perform as mechanosensors and convey signals to adjacent cells (such as osteoblasts) through the intercellular communication network.15 The major concepts regarding what is believed to be responsible for triggering bone alterations are described as strain adaptive and damage adaptive16 or a combination of these theories.17 The bone’s response induces either modeling (construction of bone) or remodeling (reconstruction of bone).18 Bone modeling results in addition or subtraction of bone. Bone remodeling is a continuous process that replaces bone and is responsible for changes in its quality, not quantity. Resorption is followed by deposition, and this process maintains the bone’s shape. Rules for Bone Adaptation to Mechanical Stimuli
According to Turner, the following three rules characterize the response of bone to stress. Bone adaptation is determined by dynamic, rather than static, loading, and it is the alteration of stress, not its consistency, that produces bone modifications; a short episode of mechanical loading is required to begin the adaptive response, and prolonging the stimulus has a decreasing effect on additional bone adaptation; and bone cells accommodate to customary 19
STORY
mechanical loading, making them less responsive to routine loading signals.19 Therefore, we can deduce that abnormal stress and strains drive structural change.19 In this regard, Graf20 reported that mastication routinely results in a repeated pattern of cyclical impact. Loading is brief, lasting about nine to 17 minutes per day. We can infer that loading of dental implants usually is dynamic. Stresses and Strains on Bone
As indicated earlier, occlusal forces on dental implants generate stresses (force acting on an object) and strains (deformation or elongation in response to stress). A variety of factors—magnitude of occlusal load, cycle number, direction and frequency—can affect the quantity of stress. The relationship between stress and strain establishes the modulus of elasticity (stiffness) of a material. In biomechanics, strain is expressed in microstrains, where 1,000 me in compression shortens bone by 0.1 percent.21 The fracture strength of lamellar bone is 25,000 me, or 2.5 percent deformity.21 According to Frost,22 a certain amount of stress is required to maintain bone homeostasis. Too little stimulation results in bone atrophy, and too much induces microfractures and bone loss. Frost22 proposed the following relationships between bone microstrain and physiological responses: microstrains from 0 to 50, atrophy; 50 to 1,500, normal bone modeling; 1,500 to 3,000, overload; > 3,000, possible destruction. Consequently, forces greater than the adaptive capacity of bone around an implant may result in osseous resorption at the bone-implant interface. Also, it is feasible that bone deformation will initiate a reparative remodeling or modeling response. This would reduce the stress and strain to a physiological level, thereby facilitating retention of implants that otherwise may have been lost. In other words, stress and strain induce a reparative process that actually lowers the perceived amount of stress because the bone becomes stronger. Threshold for Bone Loss
Some investigators demonstrated that high stress levels on bone potentially could cause bone resorption.23,24 However, it has been difficult to define a stress level that signals the induction of bone resorption around an implant. It may not be possible to delineate a specific threshold that can be applied to all patients, ABBREVIATION KEY. FEA: Finite elemental analysis. JADA 144(4)
http://jada.ada.org
Copyright © 2013 American Dental Association. All Rights Reserved.
April 2013 363
COVER
STORY
because there are many confounding variables such as loading conditions, type of prosthesis (unsplinted or splinted), angulation of abutment and implants, implant design, implant position, bone type, properties of the interface between the bone and implant, and personal genetics.25,26 Nevertheless, investigators have tried to identify a threshold for bone resorption due to stress. Using finite elemental analysis (FEA), Sugiura and colleagues27 assessed the cutoff point for bone resorption around screws. On the basis of in vivo strain measurements, they determined that the threshold was approximately -50 megapascals or 3,600 me, whereas a 40-MPa force was physiological to bone. Other researchers reported that load-bearing bones normally tolerate 4,000 me in compression and 2,500 me in tension.28-30 It appears that moderately high strains of greater than 3,000 to 4,000 me result in modest overload, and that bone is added rapidly as opposed to being resorbed when strains are greater than 4,000 me.30,31 However, we should point out that differences in bone biology might exist between species28 and between dissimilar bones within the same species.30 In addition, different study results may be due to differences in evaluation methods. Therefore, one must exercise caution in extrapolating data to the human maxilla and mandible. FEA is a helpful tool to assess theoretical responses in biological investigations, but the results may be unclear because assumptions are made concerning interactions between forces, bone and materials.26 Furthermore, application of data to diverse prosthetic situations (such as single units versus full-arch splinted prostheses) is difficult. Nevertheless, most researchers conducting FEA and other stress-related studies report increased stress on implants if angulated abutments, cantilevers, increased crown-to-root ratios, and connection of teeth to implants are used.4-6,32-34 However, these increased stresses appear to have been within physiological limits. This is supported by the finding that the survival rates of the above-described prostheses were as high as those of other prostheses that were not constructed according to designs that may cause increased stress levels.7-10 We can conclude that the increased strain was within physiological levels or that the bone adapted to decrease the strain to within tolerable limits. bone Microdamage
Fatigue. Repetitive loads (that is, cyclic fluctuating loads) applied to bone during daily activities can cause it to become fatigued; the bone then needs to be remodeled.35,36 The term 364 JADA 144(4)
http://jada.ada.org
“fatigue” denotes that the bone has lost strength and stiffness, and this deterioration is referred to as “microdamage.”37 Microdamage results in a decreased modulus of elasticity of bone and can be manifested by thinning of trabeculae and loss of connectivity between trabecular rods.38 Microdamage may contribute to formation of microcracks if remodeling fails to repair the bone. Microcracks. A microcrack is a discontinuity in the calcium-rich matrix and reflects fissures and breaks in the hydroxyapatite.39 Fazzalari and colleagues40 differentiated between microdamage and microfractures. They reported that microfracture repair is characterized by micro callus formation, a mechanism that is distinctly different from remodeling, which resolves microdamage. The amount of time required for fatigued bone with microcracks to be replaced is a function of crack growth and accumulation.41,42 Microcracks under continued loading can become macrocracks, resulting in bone fracture and bone failure. Stimulation of bone remodeling by microdamage and microcracks. When the microdamage occurs at a slow rate, bone has an opportunity to repair, and the response is referred to as “targeted remodeling.”43 In contrast, the term “random remodeling” denotes that remodeling can serve other functions such as calcium homeostasis.44 Creation of microcracks during implant procedures. Microcracks can form during creation of an osteotomy or placement of implants.45 Warreth and colleagues43 reported that drilling an osteotomy in dogs resulted in a greater number of microcracks in cortical bone than typically is found at sites where an osteotomy was not created. These authors suggested that remodeling repaired the microcracks.43 Other researchers also reported increased microcrack formation after endosseous implants were placed in bone.45,46 Given that the diameter of dental implants usually is about 0.5 millimeter larger than that of the final drill used to create an osteotomy, it is possible that increased compressive stress placed on the bone results in additional bone microfractures. Healing
Callus formation. Using a rat model, Eriksson and colleagues47 investigated similarities between bone fractures and implant healing during the first 14 days after implant placement. They suggested that creation of an osteotomy is equivalent to creating a partial fracture in bone. They identified several stages of healing: inflammation, necrotic bone removal adjacent to
April 2013
Copyright © 2013 American Dental Association. All Rights Reserved.
COVER
the implant, soft- and hard-callus formation and remodeling. Fibrin clots initially surrounded the implants, which were converted to granulation tissue (soft callus). The soft callus gradually changed to a hard callus with formation of woven bone. During remodeling, woven bone was replaced with lamellar bone.47 Mosekilde and colleagues48 found that microcalluses did not persist, because the remodeling process removed them. In this regard, Roberts49 noted that remodeling is evident at the microscopic level, but it is not visible on clinical radiographs. In humans, Trisi and Rebaudi50 found microcracks in cortical and cancellous bone around recently placed dental implants. The authors provided histological evidence of bone alterations around dental implants after application of therapeutic loads on orthodontic anchorage devices. Forces on the implants resulted in bone modeling and remodeling adjacent to the implants. The authors observed woven bone forming inside the trabecular pattern of the cancellous bone adjacent to microfractures. Histologically, they detected microcalluses— overgrowth of woven bone at stressed sites—as a response to stabilize and renew old brittle bones. This finding of microcallus formation supports the concept that microcracks are created during implant placement, and the bone adjacent to the implant undergoes remodeling. Bone’s proliferative response to stress around dental implants. Bone can respond in various ways to increased mechanical load. If the load is above a certain threshold, bone loss or loss of osseointegration can occur.51,52 If there is bone disuse, such as immobility, bone atrophy may result.53 On the other hand, if the functional load is below a destructive threshold, it can be stimulatory and induce apposition of bone and increased osseous density. Enhanced bone density has been associated with a variety of treatment scenarios, thereby supporting the concept that bone can respond to stress and modify itself to withstand increased mechanical forces. Different lines of evidence support this concept, as discussed below. dUsing computed tomography, Yunus54 assessed the level of Hounsfield units (a measure of bone density) before and after implant placement in humans. Before implant placement, the mean measurement in jaw bone was 590.7 HUs, and two months after placement, it increased to 1,035.7 HUs. dGotfredsen and colleagues55 evaluated the effect of static load on bone in maxillae and mandibles of dogs at 10 and 46 weeks. They created the load by placing expansion screws in
STORY
each quadrant. During the loading period, the authors obtained standardized radiographs and carried out fluorochrome labeling and bone biopsies. They noted increased bone density at 10 weeks, which did not increase during the next 36 weeks despite increased expansion forces. It appears that the bone reacted to the initial stress, but a prolonged loading period did not change the bone’s response. dAthletes subjected to increased bone loading (for example, playing tennis with one arm) demonstrate bone apposition.56 In contrast, people who are immobilized manifest bone loss as a result of decreased loading.53 dIn a controlled clinical trial, Appleton and colleagues57 progressively loaded dental implants and found that these implants exhibited increased peri-implant bone density in the crestal region and statistically significantly less crestal bone loss when compared with findings in implants that were not progressively loaded.57 dOrthodontic forces on dental implants result in additional bone apposition and increased osseous density.58-60 dAfter 10 months of functional loading (the test group), Berglundh and colleagues61 noted greater bone-implant contact when compared with results in unloaded implants (the control group). dIn a monkey model, bone apposition occurred when the strain level was 3,400 to 6,600 me. However, when the strain was above 6,700 me, the study results showed bone resorption and loss of bone density.62 dBarone and colleagues63 conducted a study, the results of which showed more dense bone surrounding mechanically loaded implants than that adjacent to implants that were not loaded. dBadillo-Perona and colleagues64 conducted a literature review of the peri-implant bone response in the tibia of animals when a controlled axial load was compared with a no-load force. The results of in vivo animal studies confirmed that there are benefits to immediate loading. The authors noted that early loading was associated with an increased percentage of boneto-implant contact, increased bone density and a greater amount of bone mineralization.64 They concluded that immediate loading had a beneficial effect on osseointegration, which has been confirmed in numerous studies.65 dTurner66 reported that implants placed in the patellae of horses caused trabeculae to thicken to support greater stresses. This thickening occurred without realignment of the trabeculae. We found no studies in the literature in which investigators specifically assessed alterations JADA 144(4)
http://jada.ada.org
Copyright © 2013 American Dental Association. All Rights Reserved.
April 2013 365
COVER
STORY
of osseous density after implants were restored with any of the following prosthetic constructs: cantilevered prostheses, angulated abutments, increased crown-to-root ratios, or connection of teeth to dental implants. Remodeling
Rate of normal bone remodeling. Remodeling performs several functions; it removes bone microdamage, replaces dead bone and adapts microarchitecture to stress.67 Roberts49 reported that bone apposition is an important compensating mechanism when strain surpasses the normal physiological range. In addition, Jee68 estimated that about 20 percent of the cortical and cancellous bone surfaces (endosteal and periosteal) are remodeling at any point in time. However, the rate of bone turnover appears to differ in dissimilar bones of the skeleton. Alveolar bone remodels faster than do most other bones,69,70 which might be attributed to the amount of stimulation provided by occlusal function. In general, the replacement rate of cortical bone is 7.7 percent per year, and the turnover of cancellous bone is 17.7 percent per year.71 Deguchi and colleagues72 reported that 3 percent of cortical bone and 24 percent of cancellous bone were replaced per year. It appears that investigation results can show a trend but cannot specify how much bone is remodeled each year, and this amount will vary among people. Area of remodeling around an implant. Several investigators addressed the rate of remodeling around a dental implant.73,74 Garetto and colleagues73 evaluated the response of the bone around titanium implants placed in human and animal models (rabbits, dogs and monkeys). The results showed that within 1 mm of the implants, there was a layer of bone that remodeled rapidly. The turnover rate was three to nine times faster per year within 1 mm of the implant surface than was the rate in areas farther from the implant. In this regard, Huja and colleagues75 suggested that the high rate of bone turnover results in less mineralized bone, which is more compliant than is mineralized bone. After studying the relationship between microhardness and microdamage, these authors concluded that more compliant bone helps prevent the accumulation of microdamage (microcracks). Huja and colleagues45 developed a working hypothesis (a sequence of events) about how microdamage around dental implants is managed by the body. They suggested that microdamage is produced by implant placement, microdamage initiates remodeling, callus of woven bone 366 JADA 144(4)
http://jada.ada.org
is formed, the amount of microdamage created equals the degree of microdamage repaired, and the quantity of increased bone is greater than the amount of microdamage. After assessing implants in dog femurs, Huja and colleagues45 concluded that the high success rate of implants might be caused by the rapid turnover of bone around the implant, which maintains tissue and inhibits microdamage. With respect to osseous contours, increased strain levels primarily affect bone modeling and remodeling adjacent to the medullary cavity, thereby leaving external aspects of the bone relatively unchanged.53 Trabecular patterns. The shape of bones and the trabecular patterns are determined prior to birth; however, there is plasticity at the microstructural level.76,77 After adolescence, cortical bone does not change significantly. However, despite the genetic influence,76,77 trabecular patterns can change with regard to age, function and disease.78 For example, it is apparent that patterns of trabeculae are defined before locomotor-related loading of bones, but they have the ability to remodel throughout life.79 The alterations may happen with respect to orientation of trabeculae (arrangement), but usually are concerned with changes of trabecular thickness (morphology), connectivity and spacing.79 Trabecular bone exhibits a variety of micro architectures that are related to the loadcarrying function of bone. Sites in which there is little variation (for example, vertebrae) in loading directions demonstrate unidirectional, rodlike trabecular structures.80 On the other hand, bones such as the mandible that experience loading from varying directions exhibit a more platelike trabecular architecture.80 An advantage of platelike formations is their ability to manage forces from different directions. The magnitude of the loading forces also affects the trabecular configurations. High load areas usually manifest dense platelike architecture, whereas low load areas usually demonstrate low-density rodlike structures.81 conclusions
There are two possible explanations for the success of prosthetic constructs such as cantilevered prostheses, angulated abutments, increased crown-to-implant ratios and implants connected to teeth that experience greater stress levels than those of other types of prostheses. The first is that bone is stronger than expected and can tolerate increased stress. The second is that as long as the stress/strain level does not increase beyond a threshold that causes bone destruction,
April 2013
Copyright © 2013 American Dental Association. All Rights Reserved.
COVER
bone has the ability to remodel and model and increase its osseous density, thereby adjusting to the increased stress and returning stress intensity to a physiologically acceptable level. The literature contains a paucity of data about the response of bone with regard to osseous density after implants have been placed to support the types of dental prostheses that experience additional stresses. Heretofore, the research has focused on the ability of these prosthetic constructs to avoid inducing additional bone loss. Validation of our literature review’s conclusions with postsurgical and postrestorative microcomputed tomographic scans would further clarify the concept that increased stress/strain results in increased osseous density, which, in turn, helps support the types of prostheses described earlier. n Disclosure. None of the authors reported any disclosures. 1. Andreana S, Beneduce C, Buhite R. Implant success rate in dental school setting: retrospective study. N Y State Dent J 2008;74(5): 67-70. 2. Clementini M, Morlupi A, Canullo L, Agrestini C, Barlattani A. Success rate of dental implants inserted in horizontal and vertical guided bone regenerated areas: a systematic review (published online ahead of print Apr. 26, 2012). Int J Oral Maxillofac Surg 2012;41(7): 847-852. doi:10.1016/j.ijom.2012.03.016. 3. Lang NP, Pun L, Lau KY, Li KY, Wong MC. A systematic review on survival and success rates of implants placed immediately into fresh extraction sockets after at least 1 year (published online ahead of print Dec. 28, 2011). Clin Oral Implants Res 2012;23(suppl 5):39-66. doi:10.1111/j.1600-0501.2011.02372.x. 4. Rubo JH, Capello Souza EA. Finite-element analysis of stress on dental implant prosthesis (published online ahead of print Feb. 13, 2009). Clin Implant Dent Relat Res 2010;12(2):105-113. doi:10.1111/ j.1708-8208.2008.00142.x. 5. Sadrimanesh R, Siadat H, Sadr-Eshkevari P, Monzavi A, Maurer P, Rashad A. Alveolar bone stress around implants with different abutment angulation: an FE-analysis of anterior maxilla. Implant Dent 2012;21(3):196-201. 6. Rubo JH, Souza EA. Finite element analysis of stress in bone adjacent to dental implants. J Oral Implantol 2008;34(5):248-255. 7. Greenstein G, Cavallaro JS Jr. Importance of crown to root and crown to implant ratios. Dent Today 2011;30(3):61-62, 64, 66 passim. 8. Cavallaro J Jr, Greenstein G. Angled implant abutments: a practical application of available knowledge. JADA 2011;142(2):150-158. 9. Greenstein G, Cavallaro J Jr. Cantilevers extending from unilateral implant-supported fixed prostheses: a review of the literature and presentation of practical guidelines (published correction appears in JADA 2010;141[11]:1304). JADA 2010;141(10):1221-1230. 10. Greenstein G, Cavallaro J, Smith R, Tarnow D. Connecting teeth to implants: a critical review of the literature and presentation of practical guidelines. Compend Contin Educ Dent 2009;30(7):440-453. 11. BME/ME 456 biomechanics. Mechanically mediated bone adaptation. www.engin.umich.edu/class/bme456/boneadapt/boneadapt. htm. Accessed Feb. 14, 2013. 12. Sevimay M, Turhan F, Kiliçarslan MA, Eskitascioglu G. Threedimensional finite element analysis of the effect of different bone quality on stress distribution in an implant-supported crown. J Prosthet Dent 2005;93(3):227-234. 13. Van Oosterwyck H, Duyck J, Vander Sloten J, et al. The influence of bone mechanical properties and implant fixation upon bone loading around oral implants. Clin Oral Implants Res 1998;9(6):407-418. 14. Nicolella DP, Bonewald LF, Moravits DE, Lankford J. Measure ment of microstructural strain in cortical bone. Eur J Morphol 2005;42(1-2):23-29. 15. Robling AG. The interaction of biological factors with mechanical signals in bone adaptation: recent developments (published online ahead of print April 27, 2012). Curr Osteoporos Rep 2012;10(2):126-131.
STORY
doi:10.1007/s11914-012-0099-y. 16. Sverdlova N. Tensile trabeculae: myth or reality? J Musculoskelet Neuronal Interact 2011;11(1):1-7. 17. McNamara LM, Prendergast PJ. Bone remodelling algorithms incorporating both strain and microdamage stimuli (published online ahead of print Aug. 23, 2006). J Biomech 2007;40(6):1381-1391. doi: 10.1016/j.jbiomech.2006.05.007. 18. Ruimerman R. Modeling and Remodeling in Bone Tissue (thesis). Eindhoven, Netherlands: Technische Universiteit Eindhoven; 2005:1-9. 19. Turner CH. Three rules for bone adaptation to mechanical stimuli. Bone 1998;23(5):399-407. 20. Graf H. Bruxism. Dent Clin North Am 1969;13(3):659-665. 21. Hollinger JO. Bone dynamics: morphogenesis, growth modeling, and remodeling. In: Lieberman JR, Friedlaender GE, eds. Bone Regeneration and Repair: Biology and Clinical Applications. Totowa, N.J.: Humana Press; 2005:1-19. 22. Frost HM. A 2003 update of bone physiology and Wolff ’s Law for clinicians. Angle Orthod 2004;74(1):3-15. 23. Isidor F. Influence of forces on peri-implant bone. Clin Oral Implants Res 2006;17(suppl 2):8-18. 24. Vidyasagar L, Apse P. Biological response to dental implant loading/overloading: implant overloading—empiricism or science? Stomatologija 2003;5(3):83-89. 25. Sahin S, Cehreli MC, Yalçin E. The influence of functional forces on the biomechanics of implant-supported prostheses: a review. J Dent 2002;30(7-8):271-282. 26. Geng JP, Tan KB, Liu GR. Application of finite element analysis in implant dentistry: a review of the literature. J Prosthet Dent 2001;85(6):585-598. 27. Sugiura T, Horiuchi K, Sugimura M, Tsutsumi S. Evaluation of threshold stress for bone resorption around screws based on in vivo strain measurement of miniplate. J Musculoskelet Neuronal Interact 2000;1(2):165-170. 28. Lanyon LE, Paul IL, Rubin CT, et al. In vivo strain measurements from bone and prosthesis following total hip replacement: an experimental study in sheep. J Bone Joint Surg Am 1981;63(6):989-1001. 29. Pattin CA, Caler WE, Carter DR. Cyclic mechanical property degradation during fatigue loading of cortical bone. J Biomech 1996; 29(1):69-79. 30. Burr DB, Milgrom C, Fyhrie D, et al. In vivo measurement of human tibial strains during vigorous activity. Bone 1996;18(5):405-410. 31. Frost HM. Skeletal structural adaptations to mechanical usage (SATMU), part 2: redefining Wolff ’s law—the remodeling problem. Anat Rec 1990;226(4):414-422. 32. Renouard F, Rangert B. Risk Factors in Implant Dentistry: Simplified Clinical Analysis for Predictable Treatment. Hanover Park, Ill.: Quintessence Publishing; 1999:43. 33. Brosh T, Pilo R, Sudai D. The influence of abutment angulation on strains and stresses along the implant/bone interface: comparison between two experimental techniques. J Prosthet Dent 1998;79(3):328-334. 34. Akça K, Iplikçio˘glu H. Finite element stress analysis of the effect of short implant usage in place of cantilever extensions in mandibular posterior edentulism. J Oral Rehabil 2002;29(4):350-356. 35. Herman BC, Cardoso L, Majeska RJ, Jepsen KJ, Schaffler MB. Activation of bone remodeling after fatigue: differential response to linear microcracks and diffuse damage (published online ahead of print July 12, 2010). Bone 2010;47(4):766-772. doi:10.1016/j.bone. 2010.07.006. 36. Verborgt O, Gibson GJ, Schaffler MB. Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res 2000;15(1):60-67. 37. Hazenberg JG, Hentunen TA, Heino TJ, Kurata K, Lee TC, Taylor D. Microdamage detection and repair in bone: fracture mechanics, histology, cell biology. Technol Health Care 2009;17(1):67-75. doi:10.3233/THC-2009-0536. 38. Burr DB, Turner CH, Naick P, et al. Does microdamage accumulation affect the mechanical properties of bone? J Biomech 1998;31(4):337-345. 39. Lee TC, Mohsin S, Taylor D, et al. Detecting microdamage in bone. J Anat 2003;203(2):161-172. 40. Fazzalari NL, Kuliwaba JS, Forwood MR. Cancellous bone microdamage in the proximal femur: influence of age and osteoarthritis on damage morphology and regional distribution. Bone 2002;31(6):697-702. 41. Donahue SW, Galley SA. Microdamage in bone: implications for fracture, repair, remodeling, and adaptation. Crit Rev Biomed Eng
JADA 144(4)
http://jada.ada.org
Copyright © 2013 American Dental Association. All Rights Reserved.
April 2013 367
COVER
STORY
2006;34(3):215-271. 42. O’Brien FJ, Hardiman DA, Hazenberg JG, et al. The behaviour of microcracks in compact bone. Eur J Morphol 2005;42(1-2):71-79. 43. Warreth A, Polyzois I, Lee CT, Claffey N. Generation of microdamage around endosseous implants (published online ahead of print Nov. 9, 2009). Clin Oral Implants Res 2009;20(12):1300-1306. doi:10.1111/j.1600-0501.2009.01808.x. 44. Burr DB. Targeted and nontargeted remodeling. Bone 2002; 30(1):2-4. 45. Huja SS, Katona TR, Burr DB, Garetto LP, Roberts WE. Microdamage adjacent to endosseous implants. Bone 1999;25(2):217-222. 46. Bartold PM, Kuliwaba JS, Lee V, Shah S, Marino V, Fazzalari NL. Influence of surface roughness and shape on microdamage of the osseous surface adjacent to titanium dental implants (published online ahead of print Nov. 11, 2010). Clin Oral Implants Res 2011;22(6):613-618. doi:10.1111/j.1600-0501.2010.02024.x. 47. Eriksson C, Ohlson K, Richter K, Billerdahl N, Johansson M, Nygren H. Callus formation and remodeling at titanium implants. J Biomed Mater Res A 2007;83(4):1062-1069. 48. Mosekilde L, Ebbesen EN, Tornvig L, Thomsen JS. Trabecular bone structure and strength: remodelling and repair. J Musculoskelet Neuronal Interact 2000;1(1):25-30. 49. Roberts WE. Bone physiology, metabolism, and biomechanics. In: Misch CE. Contemporary Implant Dentistry. 3rd ed. St. Louis: Mosby; 2008:557-598. 50. Trisi P, Rebaudi A. Progressive bone adaptation of titanium implants during and after orthodontic load in humans. Int J Perio dontics Restorative Dent 2002;22(1):31-43. 51. 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(2):143-152. 52. Chambrone L, Chambrone LA, Lima LA. Effects of occlusal overload on peri-implant tissue health: a systematic review of animal-model studies. J Periodontol 2010;81(10):1367-1378. doi: 10.1902/jop.2010.100176. 53. Ruff C, Holt B, Trinkaus E. Who’s afraid of the big bad Wolff?: “Wolff ’s law” and bone functional adaptation. Am J Phys Anthropol 2006;129(4):484-498. 54. Yunus B. Assessment of the increased calcification of the jaw bone with CT-Scan after dental implant placement (published online ahead of print June 23, 2011). Imaging Sci Dent 2011;41(2):59-62. doi:10.5624/isd.2011.41.2.59. 55. Gotfredsen K, Berglundh T, Lindhe J. Bone reactions adjacent to titanium implants subjected to static load of different duration: a study in the dog (III). Clin Oral Implants Res 2001;12(6):552-558. 56. Bass SL, Saxon L, Daly RM, et al. The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: a study in tennis players. J Bone Miner Res 2002;17(12):2274-2280. 57. Appleton RS, Nummikoski PV, Pigno MA, Cronin RJ, Chung KH. A radiographic assessment of progressive loading on bone around single osseointegrated implants in the posterior maxilla. Clin Oral Implants Res 2005;16(2):161-167. 58. Garat JA, Gordillo ME, Ubios AM. Bone response to different strength orthodontic forces in animals with periodontitis. J Perio dontal Res 2005;40(6):441-445. 59. Wilcko MT, Wilcko WM, Pulver JJ, Bissada NF, Bouquot JE. Accelerated osteogenic orthodontics technique: a 1-stage surgically facilitated rapid orthodontic technique with alveolar augmentation. J Oral Maxillofac Surg 2009;67(10):2149-2159. doi:10.1016/ j.joms.2009.04.095. 60. Attia MS, Shoreibah EA, Ibrahim SA, Nassar HA. Regenerative therapy of osseous defects combined with orthodontic tooth movement. J Int Acad Periodontol 2012;14(1):17-25. 61. Berglundh T, Abrahamsson I, Lindhe J. Bone reactions to longstanding functional load at implants: an experimental study in dogs. J Clin Periodontol 2005;32(9):925-932. 62. Melsen B, Lang NP. Biological reactions of alveolar bone to orthodontic loading of oral implants. Clin Oral Implants Res 2001; 12(2):144-152. 63. Barone A, Covani U, Cornelini R, Gherlone E. Radiographic bone density around immediately loaded oral implants. Clin Oral
368 JADA 144(4)
http://jada.ada.org
Implants Res 2003;14(5):610-615. 64. Badillo-Perona V, Cano-Sánchez J, Campo-Trapero J, BasconesMartinez A. Peri-implant bone mechanobiology: review of the literature. Med Oral Patol Oral Cir Bucal 2011;16(5):e677-e681. 65. Esposito M, Grusovin MG, Willings M, Coulthard P, Worthington HV. 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(6):893-904. 66. Turner CH. Biomechanical aspects of bone formation. In: Bronner F, Farach-Carson MC, eds. Bone Formation. London: Springer; 2004:83. 67. Lee CS, Szczesny SE, Soslowsky LJ. Remodeling and repair of orthopedic tissue: role of mechanical loading and biologics, part II— cartilage and bone. Am J Orthop 2011;40(3):122-128. 68. Jee WSS. Integrated bone tissue physiology: anatomy and physiology. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, Fla.: CRC Press; 2001:1-28. 69. Tricker ND, Dixon RB, Garetto LP. Cortical bone turnover and mineral apposition in dentate bone mandible. In: Garetto LP, Turner CH, Duncan RL, Burr DB, eds. Bridging the Gap Between Dental and Orthopaedic Implants: Proceedings of the 3rd Annual Indiana Conference, Indianapolis, Indiana. Indianapolis: Indiana University School of Dentistry; 2002:226-227. 70. Huja SS, Fernandez SA, Hill KJ, Li Y. Remodeling dynamics in the alveolar process in skeletally mature dogs. Anat Rec A Discov Mol Cell Evol Biol 2006;288(12):1243-1249. 71. Garnero P, Szulic DA. Bone remodeling: cellular activities in bone. In: Orwoll ES, Bilezikian JP, Vanderschueren D, eds. Osteoporosis in Men: The Effects of Gender on Skeletal Health. 2nd ed. London: Elsevier; 2010:25-40. 72. Deguchi T, Takano-Yamamoto T, Yabuuchi T, Ando R, Roberts WE, Garetto LP. Histomorphometric evaluation of alveolar bone turnover between the maxilla and the mandible during experimental tooth movement in dogs. Am J Orthod Dentofacial Orthop 2008;133(6):889-897. doi:10.1016/j.ajodo.2006.12.013. 73. Garetto LP, Chen J, Parr JA, Roberts WE. Remodeling dynamics of bone supporting rigidly fixed titanium implants: a histomorphometric comparison in four species including humans. Implant Dent 1995;4(4):235-243. 74. Chen J, Chen K, Garetto LP, Roberts WE. Mechanical response to functional and therapeutic loading of a retromolar endosseous implant used for orthodontic anchorage to mesially translate mandibular molars. Implant Dent 1995;4(4):246-258. 75. Huja SS, Katona TR, Moore BK, Roberts WE. Microhardness and anisotropy of the vital osseous interface and endosseous implant supporting bone. J Orthop Res 1998;16(1):54-60. 76. Cunningham CA, Black SM. Anticipating bipedalism: trabecular organization in the newborn ilium (published online ahead of print May 22, 2009). J Anat 2009;214(6):817-829. doi:10.1111/j.1469-7580. 2009.01073.x. 77. Cunningham CA, Black SM. The neonatal ilium: metaphyseal drivers and vascular passengers (published online ahead of print May 17, 2010). Anat Rec (Hoboken) 2010;293(8):1297-1309. doi:10.1002/ ar.21182. 78. Tanck E, Homminga J, van Lenthe GH, Huiskes R. Increase in bone volume fraction precedes architectural adaptation in growing bone. Bone 2001;28(6):650-654. 79. Abel R, Macho GA. Ontogenetic changes in the internal and external morphology of the ilium in modern humans (published online ahead of print Feb. 17, 2011). J Anat 2011;218(3):324-335. doi:10.1111/ j.1469-7580.2011.01342.x. 80. Christen P, van Rietbergen B, Lambers FM, Müller R, Ito K. Bone morphology allows estimation of loading history in a murine model of bone adaptation (published online ahead of print July 7, 2011). Biomech Model Mechanobiol 2012;11(3-4):483-492. doi:10.1007/ s10237-011-0327-x. 81. Ding M, Odgaard A, Danielsen CC, Hvid I. Mutual associations among microstructural, physical and mechanical properties of human cancellous bone. J Bone Joint Surg Br 2002;84(6):900-907.
April 2013
Copyright © 2013 American Dental Association. All Rights Reserved.
STORY
Assessing bone’s adaptive capacity around dental implants A literature review Gary Greenstein, DDS, MS; John Cavallaro, DDS; Dennis Tarnow, DDS
D
ental implants are an integral facet of restorative therapy and have a high survival rate.1-3 However, researchers and clinicians are concerned that certain types or aspects of prosthetic restorations supported by dental implants (such as cantilevered prostheses, angulated abutments, prostheses with increased crown-to-implant ratios, implants connected to teeth) are associated with increased stress,4-6 which may reduce their survival rates. In this regard, the above prosthetic constructs have not demonstrated increased failure rates when compared with the rate of implant loss associated with prosthetic constructs that are not exposed to increased stress.7-10 With respect to prosthetic constructs that experience increased stress, several authors have provided clinical guidelines regarding ways to enhance clinical success.7-10 Therefore, it is important that clinicians be familiar with contemporary perspectives concerning the bone’s response to placement of dental implants. We review concepts pertaining to bone adaptation that 362 JADA 144(4)
http://jada.ada.org
AB STRACT Background. Increased stress (force) on prostheses induces strain (deformation) in the peri-implant bone. Elevated stress and strain could result in the failure of implants that support prostheses. However, the survival rate of implants supporting prostheses under increased stress is high. Either the bone is stronger than expected or it adapts to increased stress. Concepts regarding bone’s adaptive capacity continue to evolve and are the focus of this literature review. Types of Studies Reviewed. The authors searched the literature to find studies that addressed the bone’s capacity to adjust to increased stress and strain. They assessed experimental and clinical trials in which investigators monitored healing after placement of dental implants. Results. The data indicate that forces greater than the bone’s adaptive ability can induce loss of osseointegration, as well as osseous resorption. In contrast, it is possible that increased stress on prostheses initiates a reparative process, thereby facilitating retention of implants experiencing increased stress. Numerous lines of evidence support the concept that bone can modify itself to withstand increased mechanical forces. Practical Implications. The authors provide an explanation for the high success rate of prostheses and implants in bone that are exposed to increased stress and strain. Key Words. Bone; dental implants; osseointegration; resorption. JADA 2013;144(4):362-368. Dr. Greenstein is a clinical professor, Department of Periodontology, College of Dental Medicine, Columbia University, New York City, and is in private practice in Freehold, N.J. Address reprint requests to Dr. Greenstein, 900 W. Main St., Freehold, N.J. 07728, e-mail [email protected]. Dr. Cavallaro is an associate clinical professor, Department of Prosthodontics, and director, Implant Fellowship Program, College of Dental Medicine, Columbia University, New York City, and is in private practice in Brooklyn, N.Y. Dr. Tarnow is director of dental implant education and a clinical professor, Department of Periodontology, College of Dental Medicine, Columbia University, New York City, and is in private practice in New York City.
April 2013
Copyright © 2013 American Dental Association. All Rights Reserved.
COVER
may account for high survival rates of prostheses that are subjected to increased stresses. Bone Mechanotransduction
Bone mechanotransduction is the mechanism that permits bone to detect stimuli, but this process is not understood completely. It is thought that bone cells sense and respond to their mechanical environment by changing their biological and biochemical actions.11 We need to underscore that it is the strain (deformation or elongation in response to stress), not stress (force acting on bone), that precipitates alteration of the bone’s response.11 In this regard, stress and strain concentrations are affected by bone quality; dense bone is more resistant to deformation than is less dense bone.12 In addition, other factors can affect the strain response, such as the bone-implant interface and bone elasticity.13 Osteocytes are thought to respond to one of three possible stimuli: direct mechanical stimulation, fluid flow induced by shear stress or bone microdamage.14 The prevailing concept suggests that under dynamic loading, bone matrix deformation produces an interstitial fluid flow in the lacunocanalicular system.14 This fluid creates shear stress that stimulates osteocytes. Osteocytes perform as mechanosensors and convey signals to adjacent cells (such as osteoblasts) through the intercellular communication network.15 The major concepts regarding what is believed to be responsible for triggering bone alterations are described as strain adaptive and damage adaptive16 or a combination of these theories.17 The bone’s response induces either modeling (construction of bone) or remodeling (reconstruction of bone).18 Bone modeling results in addition or subtraction of bone. Bone remodeling is a continuous process that replaces bone and is responsible for changes in its quality, not quantity. Resorption is followed by deposition, and this process maintains the bone’s shape. Rules for Bone Adaptation to Mechanical Stimuli
According to Turner, the following three rules characterize the response of bone to stress. Bone adaptation is determined by dynamic, rather than static, loading, and it is the alteration of stress, not its consistency, that produces bone modifications; a short episode of mechanical loading is required to begin the adaptive response, and prolonging the stimulus has a decreasing effect on additional bone adaptation; and bone cells accommodate to customary 19
STORY
mechanical loading, making them less responsive to routine loading signals.19 Therefore, we can deduce that abnormal stress and strains drive structural change.19 In this regard, Graf20 reported that mastication routinely results in a repeated pattern of cyclical impact. Loading is brief, lasting about nine to 17 minutes per day. We can infer that loading of dental implants usually is dynamic. Stresses and Strains on Bone
As indicated earlier, occlusal forces on dental implants generate stresses (force acting on an object) and strains (deformation or elongation in response to stress). A variety of factors—magnitude of occlusal load, cycle number, direction and frequency—can affect the quantity of stress. The relationship between stress and strain establishes the modulus of elasticity (stiffness) of a material. In biomechanics, strain is expressed in microstrains, where 1,000 me in compression shortens bone by 0.1 percent.21 The fracture strength of lamellar bone is 25,000 me, or 2.5 percent deformity.21 According to Frost,22 a certain amount of stress is required to maintain bone homeostasis. Too little stimulation results in bone atrophy, and too much induces microfractures and bone loss. Frost22 proposed the following relationships between bone microstrain and physiological responses: microstrains from 0 to 50, atrophy; 50 to 1,500, normal bone modeling; 1,500 to 3,000, overload; > 3,000, possible destruction. Consequently, forces greater than the adaptive capacity of bone around an implant may result in osseous resorption at the bone-implant interface. Also, it is feasible that bone deformation will initiate a reparative remodeling or modeling response. This would reduce the stress and strain to a physiological level, thereby facilitating retention of implants that otherwise may have been lost. In other words, stress and strain induce a reparative process that actually lowers the perceived amount of stress because the bone becomes stronger. Threshold for Bone Loss
Some investigators demonstrated that high stress levels on bone potentially could cause bone resorption.23,24 However, it has been difficult to define a stress level that signals the induction of bone resorption around an implant. It may not be possible to delineate a specific threshold that can be applied to all patients, ABBREVIATION KEY. FEA: Finite elemental analysis. JADA 144(4)
http://jada.ada.org
Copyright © 2013 American Dental Association. All Rights Reserved.
April 2013 363
COVER
STORY
because there are many confounding variables such as loading conditions, type of prosthesis (unsplinted or splinted), angulation of abutment and implants, implant design, implant position, bone type, properties of the interface between the bone and implant, and personal genetics.25,26 Nevertheless, investigators have tried to identify a threshold for bone resorption due to stress. Using finite elemental analysis (FEA), Sugiura and colleagues27 assessed the cutoff point for bone resorption around screws. On the basis of in vivo strain measurements, they determined that the threshold was approximately -50 megapascals or 3,600 me, whereas a 40-MPa force was physiological to bone. Other researchers reported that load-bearing bones normally tolerate 4,000 me in compression and 2,500 me in tension.28-30 It appears that moderately high strains of greater than 3,000 to 4,000 me result in modest overload, and that bone is added rapidly as opposed to being resorbed when strains are greater than 4,000 me.30,31 However, we should point out that differences in bone biology might exist between species28 and between dissimilar bones within the same species.30 In addition, different study results may be due to differences in evaluation methods. Therefore, one must exercise caution in extrapolating data to the human maxilla and mandible. FEA is a helpful tool to assess theoretical responses in biological investigations, but the results may be unclear because assumptions are made concerning interactions between forces, bone and materials.26 Furthermore, application of data to diverse prosthetic situations (such as single units versus full-arch splinted prostheses) is difficult. Nevertheless, most researchers conducting FEA and other stress-related studies report increased stress on implants if angulated abutments, cantilevers, increased crown-to-root ratios, and connection of teeth to implants are used.4-6,32-34 However, these increased stresses appear to have been within physiological limits. This is supported by the finding that the survival rates of the above-described prostheses were as high as those of other prostheses that were not constructed according to designs that may cause increased stress levels.7-10 We can conclude that the increased strain was within physiological levels or that the bone adapted to decrease the strain to within tolerable limits. bone Microdamage
Fatigue. Repetitive loads (that is, cyclic fluctuating loads) applied to bone during daily activities can cause it to become fatigued; the bone then needs to be remodeled.35,36 The term 364 JADA 144(4)
http://jada.ada.org
“fatigue” denotes that the bone has lost strength and stiffness, and this deterioration is referred to as “microdamage.”37 Microdamage results in a decreased modulus of elasticity of bone and can be manifested by thinning of trabeculae and loss of connectivity between trabecular rods.38 Microdamage may contribute to formation of microcracks if remodeling fails to repair the bone. Microcracks. A microcrack is a discontinuity in the calcium-rich matrix and reflects fissures and breaks in the hydroxyapatite.39 Fazzalari and colleagues40 differentiated between microdamage and microfractures. They reported that microfracture repair is characterized by micro callus formation, a mechanism that is distinctly different from remodeling, which resolves microdamage. The amount of time required for fatigued bone with microcracks to be replaced is a function of crack growth and accumulation.41,42 Microcracks under continued loading can become macrocracks, resulting in bone fracture and bone failure. Stimulation of bone remodeling by microdamage and microcracks. When the microdamage occurs at a slow rate, bone has an opportunity to repair, and the response is referred to as “targeted remodeling.”43 In contrast, the term “random remodeling” denotes that remodeling can serve other functions such as calcium homeostasis.44 Creation of microcracks during implant procedures. Microcracks can form during creation of an osteotomy or placement of implants.45 Warreth and colleagues43 reported that drilling an osteotomy in dogs resulted in a greater number of microcracks in cortical bone than typically is found at sites where an osteotomy was not created. These authors suggested that remodeling repaired the microcracks.43 Other researchers also reported increased microcrack formation after endosseous implants were placed in bone.45,46 Given that the diameter of dental implants usually is about 0.5 millimeter larger than that of the final drill used to create an osteotomy, it is possible that increased compressive stress placed on the bone results in additional bone microfractures. Healing
Callus formation. Using a rat model, Eriksson and colleagues47 investigated similarities between bone fractures and implant healing during the first 14 days after implant placement. They suggested that creation of an osteotomy is equivalent to creating a partial fracture in bone. They identified several stages of healing: inflammation, necrotic bone removal adjacent to
April 2013
Copyright © 2013 American Dental Association. All Rights Reserved.
COVER
the implant, soft- and hard-callus formation and remodeling. Fibrin clots initially surrounded the implants, which were converted to granulation tissue (soft callus). The soft callus gradually changed to a hard callus with formation of woven bone. During remodeling, woven bone was replaced with lamellar bone.47 Mosekilde and colleagues48 found that microcalluses did not persist, because the remodeling process removed them. In this regard, Roberts49 noted that remodeling is evident at the microscopic level, but it is not visible on clinical radiographs. In humans, Trisi and Rebaudi50 found microcracks in cortical and cancellous bone around recently placed dental implants. The authors provided histological evidence of bone alterations around dental implants after application of therapeutic loads on orthodontic anchorage devices. Forces on the implants resulted in bone modeling and remodeling adjacent to the implants. The authors observed woven bone forming inside the trabecular pattern of the cancellous bone adjacent to microfractures. Histologically, they detected microcalluses— overgrowth of woven bone at stressed sites—as a response to stabilize and renew old brittle bones. This finding of microcallus formation supports the concept that microcracks are created during implant placement, and the bone adjacent to the implant undergoes remodeling. Bone’s proliferative response to stress around dental implants. Bone can respond in various ways to increased mechanical load. If the load is above a certain threshold, bone loss or loss of osseointegration can occur.51,52 If there is bone disuse, such as immobility, bone atrophy may result.53 On the other hand, if the functional load is below a destructive threshold, it can be stimulatory and induce apposition of bone and increased osseous density. Enhanced bone density has been associated with a variety of treatment scenarios, thereby supporting the concept that bone can respond to stress and modify itself to withstand increased mechanical forces. Different lines of evidence support this concept, as discussed below. dUsing computed tomography, Yunus54 assessed the level of Hounsfield units (a measure of bone density) before and after implant placement in humans. Before implant placement, the mean measurement in jaw bone was 590.7 HUs, and two months after placement, it increased to 1,035.7 HUs. dGotfredsen and colleagues55 evaluated the effect of static load on bone in maxillae and mandibles of dogs at 10 and 46 weeks. They created the load by placing expansion screws in
STORY
each quadrant. During the loading period, the authors obtained standardized radiographs and carried out fluorochrome labeling and bone biopsies. They noted increased bone density at 10 weeks, which did not increase during the next 36 weeks despite increased expansion forces. It appears that the bone reacted to the initial stress, but a prolonged loading period did not change the bone’s response. dAthletes subjected to increased bone loading (for example, playing tennis with one arm) demonstrate bone apposition.56 In contrast, people who are immobilized manifest bone loss as a result of decreased loading.53 dIn a controlled clinical trial, Appleton and colleagues57 progressively loaded dental implants and found that these implants exhibited increased peri-implant bone density in the crestal region and statistically significantly less crestal bone loss when compared with findings in implants that were not progressively loaded.57 dOrthodontic forces on dental implants result in additional bone apposition and increased osseous density.58-60 dAfter 10 months of functional loading (the test group), Berglundh and colleagues61 noted greater bone-implant contact when compared with results in unloaded implants (the control group). dIn a monkey model, bone apposition occurred when the strain level was 3,400 to 6,600 me. However, when the strain was above 6,700 me, the study results showed bone resorption and loss of bone density.62 dBarone and colleagues63 conducted a study, the results of which showed more dense bone surrounding mechanically loaded implants than that adjacent to implants that were not loaded. dBadillo-Perona and colleagues64 conducted a literature review of the peri-implant bone response in the tibia of animals when a controlled axial load was compared with a no-load force. The results of in vivo animal studies confirmed that there are benefits to immediate loading. The authors noted that early loading was associated with an increased percentage of boneto-implant contact, increased bone density and a greater amount of bone mineralization.64 They concluded that immediate loading had a beneficial effect on osseointegration, which has been confirmed in numerous studies.65 dTurner66 reported that implants placed in the patellae of horses caused trabeculae to thicken to support greater stresses. This thickening occurred without realignment of the trabeculae. We found no studies in the literature in which investigators specifically assessed alterations JADA 144(4)
http://jada.ada.org
Copyright © 2013 American Dental Association. All Rights Reserved.
April 2013 365
COVER
STORY
of osseous density after implants were restored with any of the following prosthetic constructs: cantilevered prostheses, angulated abutments, increased crown-to-root ratios, or connection of teeth to dental implants. Remodeling
Rate of normal bone remodeling. Remodeling performs several functions; it removes bone microdamage, replaces dead bone and adapts microarchitecture to stress.67 Roberts49 reported that bone apposition is an important compensating mechanism when strain surpasses the normal physiological range. In addition, Jee68 estimated that about 20 percent of the cortical and cancellous bone surfaces (endosteal and periosteal) are remodeling at any point in time. However, the rate of bone turnover appears to differ in dissimilar bones of the skeleton. Alveolar bone remodels faster than do most other bones,69,70 which might be attributed to the amount of stimulation provided by occlusal function. In general, the replacement rate of cortical bone is 7.7 percent per year, and the turnover of cancellous bone is 17.7 percent per year.71 Deguchi and colleagues72 reported that 3 percent of cortical bone and 24 percent of cancellous bone were replaced per year. It appears that investigation results can show a trend but cannot specify how much bone is remodeled each year, and this amount will vary among people. Area of remodeling around an implant. Several investigators addressed the rate of remodeling around a dental implant.73,74 Garetto and colleagues73 evaluated the response of the bone around titanium implants placed in human and animal models (rabbits, dogs and monkeys). The results showed that within 1 mm of the implants, there was a layer of bone that remodeled rapidly. The turnover rate was three to nine times faster per year within 1 mm of the implant surface than was the rate in areas farther from the implant. In this regard, Huja and colleagues75 suggested that the high rate of bone turnover results in less mineralized bone, which is more compliant than is mineralized bone. After studying the relationship between microhardness and microdamage, these authors concluded that more compliant bone helps prevent the accumulation of microdamage (microcracks). Huja and colleagues45 developed a working hypothesis (a sequence of events) about how microdamage around dental implants is managed by the body. They suggested that microdamage is produced by implant placement, microdamage initiates remodeling, callus of woven bone 366 JADA 144(4)
http://jada.ada.org
is formed, the amount of microdamage created equals the degree of microdamage repaired, and the quantity of increased bone is greater than the amount of microdamage. After assessing implants in dog femurs, Huja and colleagues45 concluded that the high success rate of implants might be caused by the rapid turnover of bone around the implant, which maintains tissue and inhibits microdamage. With respect to osseous contours, increased strain levels primarily affect bone modeling and remodeling adjacent to the medullary cavity, thereby leaving external aspects of the bone relatively unchanged.53 Trabecular patterns. The shape of bones and the trabecular patterns are determined prior to birth; however, there is plasticity at the microstructural level.76,77 After adolescence, cortical bone does not change significantly. However, despite the genetic influence,76,77 trabecular patterns can change with regard to age, function and disease.78 For example, it is apparent that patterns of trabeculae are defined before locomotor-related loading of bones, but they have the ability to remodel throughout life.79 The alterations may happen with respect to orientation of trabeculae (arrangement), but usually are concerned with changes of trabecular thickness (morphology), connectivity and spacing.79 Trabecular bone exhibits a variety of micro architectures that are related to the loadcarrying function of bone. Sites in which there is little variation (for example, vertebrae) in loading directions demonstrate unidirectional, rodlike trabecular structures.80 On the other hand, bones such as the mandible that experience loading from varying directions exhibit a more platelike trabecular architecture.80 An advantage of platelike formations is their ability to manage forces from different directions. The magnitude of the loading forces also affects the trabecular configurations. High load areas usually manifest dense platelike architecture, whereas low load areas usually demonstrate low-density rodlike structures.81 conclusions
There are two possible explanations for the success of prosthetic constructs such as cantilevered prostheses, angulated abutments, increased crown-to-implant ratios and implants connected to teeth that experience greater stress levels than those of other types of prostheses. The first is that bone is stronger than expected and can tolerate increased stress. The second is that as long as the stress/strain level does not increase beyond a threshold that causes bone destruction,
April 2013
Copyright © 2013 American Dental Association. All Rights Reserved.
COVER
bone has the ability to remodel and model and increase its osseous density, thereby adjusting to the increased stress and returning stress intensity to a physiologically acceptable level. The literature contains a paucity of data about the response of bone with regard to osseous density after implants have been placed to support the types of dental prostheses that experience additional stresses. Heretofore, the research has focused on the ability of these prosthetic constructs to avoid inducing additional bone loss. Validation of our literature review’s conclusions with postsurgical and postrestorative microcomputed tomographic scans would further clarify the concept that increased stress/strain results in increased osseous density, which, in turn, helps support the types of prostheses described earlier. n Disclosure. None of the authors reported any disclosures. 1. Andreana S, Beneduce C, Buhite R. Implant success rate in dental school setting: retrospective study. N Y State Dent J 2008;74(5): 67-70. 2. Clementini M, Morlupi A, Canullo L, Agrestini C, Barlattani A. Success rate of dental implants inserted in horizontal and vertical guided bone regenerated areas: a systematic review (published online ahead of print Apr. 26, 2012). Int J Oral Maxillofac Surg 2012;41(7): 847-852. doi:10.1016/j.ijom.2012.03.016. 3. Lang NP, Pun L, Lau KY, Li KY, Wong MC. A systematic review on survival and success rates of implants placed immediately into fresh extraction sockets after at least 1 year (published online ahead of print Dec. 28, 2011). Clin Oral Implants Res 2012;23(suppl 5):39-66. doi:10.1111/j.1600-0501.2011.02372.x. 4. Rubo JH, Capello Souza EA. Finite-element analysis of stress on dental implant prosthesis (published online ahead of print Feb. 13, 2009). Clin Implant Dent Relat Res 2010;12(2):105-113. doi:10.1111/ j.1708-8208.2008.00142.x. 5. Sadrimanesh R, Siadat H, Sadr-Eshkevari P, Monzavi A, Maurer P, Rashad A. Alveolar bone stress around implants with different abutment angulation: an FE-analysis of anterior maxilla. Implant Dent 2012;21(3):196-201. 6. Rubo JH, Souza EA. Finite element analysis of stress in bone adjacent to dental implants. J Oral Implantol 2008;34(5):248-255. 7. Greenstein G, Cavallaro JS Jr. Importance of crown to root and crown to implant ratios. Dent Today 2011;30(3):61-62, 64, 66 passim. 8. Cavallaro J Jr, Greenstein G. Angled implant abutments: a practical application of available knowledge. JADA 2011;142(2):150-158. 9. Greenstein G, Cavallaro J Jr. Cantilevers extending from unilateral implant-supported fixed prostheses: a review of the literature and presentation of practical guidelines (published correction appears in JADA 2010;141[11]:1304). JADA 2010;141(10):1221-1230. 10. Greenstein G, Cavallaro J, Smith R, Tarnow D. Connecting teeth to implants: a critical review of the literature and presentation of practical guidelines. Compend Contin Educ Dent 2009;30(7):440-453. 11. BME/ME 456 biomechanics. Mechanically mediated bone adaptation. www.engin.umich.edu/class/bme456/boneadapt/boneadapt. htm. Accessed Feb. 14, 2013. 12. Sevimay M, Turhan F, Kiliçarslan MA, Eskitascioglu G. Threedimensional finite element analysis of the effect of different bone quality on stress distribution in an implant-supported crown. J Prosthet Dent 2005;93(3):227-234. 13. Van Oosterwyck H, Duyck J, Vander Sloten J, et al. The influence of bone mechanical properties and implant fixation upon bone loading around oral implants. Clin Oral Implants Res 1998;9(6):407-418. 14. Nicolella DP, Bonewald LF, Moravits DE, Lankford J. Measure ment of microstructural strain in cortical bone. Eur J Morphol 2005;42(1-2):23-29. 15. Robling AG. The interaction of biological factors with mechanical signals in bone adaptation: recent developments (published online ahead of print April 27, 2012). Curr Osteoporos Rep 2012;10(2):126-131.
STORY
doi:10.1007/s11914-012-0099-y. 16. Sverdlova N. Tensile trabeculae: myth or reality? J Musculoskelet Neuronal Interact 2011;11(1):1-7. 17. McNamara LM, Prendergast PJ. Bone remodelling algorithms incorporating both strain and microdamage stimuli (published online ahead of print Aug. 23, 2006). J Biomech 2007;40(6):1381-1391. doi: 10.1016/j.jbiomech.2006.05.007. 18. Ruimerman R. Modeling and Remodeling in Bone Tissue (thesis). Eindhoven, Netherlands: Technische Universiteit Eindhoven; 2005:1-9. 19. Turner CH. Three rules for bone adaptation to mechanical stimuli. Bone 1998;23(5):399-407. 20. Graf H. Bruxism. Dent Clin North Am 1969;13(3):659-665. 21. Hollinger JO. Bone dynamics: morphogenesis, growth modeling, and remodeling. In: Lieberman JR, Friedlaender GE, eds. Bone Regeneration and Repair: Biology and Clinical Applications. Totowa, N.J.: Humana Press; 2005:1-19. 22. Frost HM. A 2003 update of bone physiology and Wolff ’s Law for clinicians. Angle Orthod 2004;74(1):3-15. 23. Isidor F. Influence of forces on peri-implant bone. Clin Oral Implants Res 2006;17(suppl 2):8-18. 24. Vidyasagar L, Apse P. Biological response to dental implant loading/overloading: implant overloading—empiricism or science? Stomatologija 2003;5(3):83-89. 25. Sahin S, Cehreli MC, Yalçin E. The influence of functional forces on the biomechanics of implant-supported prostheses: a review. J Dent 2002;30(7-8):271-282. 26. Geng JP, Tan KB, Liu GR. Application of finite element analysis in implant dentistry: a review of the literature. J Prosthet Dent 2001;85(6):585-598. 27. Sugiura T, Horiuchi K, Sugimura M, Tsutsumi S. Evaluation of threshold stress for bone resorption around screws based on in vivo strain measurement of miniplate. J Musculoskelet Neuronal Interact 2000;1(2):165-170. 28. Lanyon LE, Paul IL, Rubin CT, et al. In vivo strain measurements from bone and prosthesis following total hip replacement: an experimental study in sheep. J Bone Joint Surg Am 1981;63(6):989-1001. 29. Pattin CA, Caler WE, Carter DR. Cyclic mechanical property degradation during fatigue loading of cortical bone. J Biomech 1996; 29(1):69-79. 30. Burr DB, Milgrom C, Fyhrie D, et al. In vivo measurement of human tibial strains during vigorous activity. Bone 1996;18(5):405-410. 31. Frost HM. Skeletal structural adaptations to mechanical usage (SATMU), part 2: redefining Wolff ’s law—the remodeling problem. Anat Rec 1990;226(4):414-422. 32. Renouard F, Rangert B. Risk Factors in Implant Dentistry: Simplified Clinical Analysis for Predictable Treatment. Hanover Park, Ill.: Quintessence Publishing; 1999:43. 33. Brosh T, Pilo R, Sudai D. The influence of abutment angulation on strains and stresses along the implant/bone interface: comparison between two experimental techniques. J Prosthet Dent 1998;79(3):328-334. 34. Akça K, Iplikçio˘glu H. Finite element stress analysis of the effect of short implant usage in place of cantilever extensions in mandibular posterior edentulism. J Oral Rehabil 2002;29(4):350-356. 35. Herman BC, Cardoso L, Majeska RJ, Jepsen KJ, Schaffler MB. Activation of bone remodeling after fatigue: differential response to linear microcracks and diffuse damage (published online ahead of print July 12, 2010). Bone 2010;47(4):766-772. doi:10.1016/j.bone. 2010.07.006. 36. Verborgt O, Gibson GJ, Schaffler MB. Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res 2000;15(1):60-67. 37. Hazenberg JG, Hentunen TA, Heino TJ, Kurata K, Lee TC, Taylor D. Microdamage detection and repair in bone: fracture mechanics, histology, cell biology. Technol Health Care 2009;17(1):67-75. doi:10.3233/THC-2009-0536. 38. Burr DB, Turner CH, Naick P, et al. Does microdamage accumulation affect the mechanical properties of bone? J Biomech 1998;31(4):337-345. 39. Lee TC, Mohsin S, Taylor D, et al. Detecting microdamage in bone. J Anat 2003;203(2):161-172. 40. Fazzalari NL, Kuliwaba JS, Forwood MR. Cancellous bone microdamage in the proximal femur: influence of age and osteoarthritis on damage morphology and regional distribution. Bone 2002;31(6):697-702. 41. Donahue SW, Galley SA. Microdamage in bone: implications for fracture, repair, remodeling, and adaptation. Crit Rev Biomed Eng
JADA 144(4)
http://jada.ada.org
Copyright © 2013 American Dental Association. All Rights Reserved.
April 2013 367
COVER
STORY
2006;34(3):215-271. 42. O’Brien FJ, Hardiman DA, Hazenberg JG, et al. The behaviour of microcracks in compact bone. Eur J Morphol 2005;42(1-2):71-79. 43. Warreth A, Polyzois I, Lee CT, Claffey N. Generation of microdamage around endosseous implants (published online ahead of print Nov. 9, 2009). Clin Oral Implants Res 2009;20(12):1300-1306. doi:10.1111/j.1600-0501.2009.01808.x. 44. Burr DB. Targeted and nontargeted remodeling. Bone 2002; 30(1):2-4. 45. Huja SS, Katona TR, Burr DB, Garetto LP, Roberts WE. Microdamage adjacent to endosseous implants. Bone 1999;25(2):217-222. 46. Bartold PM, Kuliwaba JS, Lee V, Shah S, Marino V, Fazzalari NL. Influence of surface roughness and shape on microdamage of the osseous surface adjacent to titanium dental implants (published online ahead of print Nov. 11, 2010). Clin Oral Implants Res 2011;22(6):613-618. doi:10.1111/j.1600-0501.2010.02024.x. 47. Eriksson C, Ohlson K, Richter K, Billerdahl N, Johansson M, Nygren H. Callus formation and remodeling at titanium implants. J Biomed Mater Res A 2007;83(4):1062-1069. 48. Mosekilde L, Ebbesen EN, Tornvig L, Thomsen JS. Trabecular bone structure and strength: remodelling and repair. J Musculoskelet Neuronal Interact 2000;1(1):25-30. 49. Roberts WE. Bone physiology, metabolism, and biomechanics. In: Misch CE. Contemporary Implant Dentistry. 3rd ed. St. Louis: Mosby; 2008:557-598. 50. Trisi P, Rebaudi A. Progressive bone adaptation of titanium implants during and after orthodontic load in humans. Int J Perio dontics Restorative Dent 2002;22(1):31-43. 51. 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(2):143-152. 52. Chambrone L, Chambrone LA, Lima LA. Effects of occlusal overload on peri-implant tissue health: a systematic review of animal-model studies. J Periodontol 2010;81(10):1367-1378. doi: 10.1902/jop.2010.100176. 53. Ruff C, Holt B, Trinkaus E. Who’s afraid of the big bad Wolff?: “Wolff ’s law” and bone functional adaptation. Am J Phys Anthropol 2006;129(4):484-498. 54. Yunus B. Assessment of the increased calcification of the jaw bone with CT-Scan after dental implant placement (published online ahead of print June 23, 2011). Imaging Sci Dent 2011;41(2):59-62. doi:10.5624/isd.2011.41.2.59. 55. Gotfredsen K, Berglundh T, Lindhe J. Bone reactions adjacent to titanium implants subjected to static load of different duration: a study in the dog (III). Clin Oral Implants Res 2001;12(6):552-558. 56. Bass SL, Saxon L, Daly RM, et al. The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: a study in tennis players. J Bone Miner Res 2002;17(12):2274-2280. 57. Appleton RS, Nummikoski PV, Pigno MA, Cronin RJ, Chung KH. A radiographic assessment of progressive loading on bone around single osseointegrated implants in the posterior maxilla. Clin Oral Implants Res 2005;16(2):161-167. 58. Garat JA, Gordillo ME, Ubios AM. Bone response to different strength orthodontic forces in animals with periodontitis. J Perio dontal Res 2005;40(6):441-445. 59. Wilcko MT, Wilcko WM, Pulver JJ, Bissada NF, Bouquot JE. Accelerated osteogenic orthodontics technique: a 1-stage surgically facilitated rapid orthodontic technique with alveolar augmentation. J Oral Maxillofac Surg 2009;67(10):2149-2159. doi:10.1016/ j.joms.2009.04.095. 60. Attia MS, Shoreibah EA, Ibrahim SA, Nassar HA. Regenerative therapy of osseous defects combined with orthodontic tooth movement. J Int Acad Periodontol 2012;14(1):17-25. 61. Berglundh T, Abrahamsson I, Lindhe J. Bone reactions to longstanding functional load at implants: an experimental study in dogs. J Clin Periodontol 2005;32(9):925-932. 62. Melsen B, Lang NP. Biological reactions of alveolar bone to orthodontic loading of oral implants. Clin Oral Implants Res 2001; 12(2):144-152. 63. Barone A, Covani U, Cornelini R, Gherlone E. Radiographic bone density around immediately loaded oral implants. Clin Oral
368 JADA 144(4)
http://jada.ada.org
Implants Res 2003;14(5):610-615. 64. Badillo-Perona V, Cano-Sánchez J, Campo-Trapero J, BasconesMartinez A. Peri-implant bone mechanobiology: review of the literature. Med Oral Patol Oral Cir Bucal 2011;16(5):e677-e681. 65. Esposito M, Grusovin MG, Willings M, Coulthard P, Worthington HV. 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(6):893-904. 66. Turner CH. Biomechanical aspects of bone formation. In: Bronner F, Farach-Carson MC, eds. Bone Formation. London: Springer; 2004:83. 67. Lee CS, Szczesny SE, Soslowsky LJ. Remodeling and repair of orthopedic tissue: role of mechanical loading and biologics, part II— cartilage and bone. Am J Orthop 2011;40(3):122-128. 68. Jee WSS. Integrated bone tissue physiology: anatomy and physiology. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, Fla.: CRC Press; 2001:1-28. 69. Tricker ND, Dixon RB, Garetto LP. Cortical bone turnover and mineral apposition in dentate bone mandible. In: Garetto LP, Turner CH, Duncan RL, Burr DB, eds. Bridging the Gap Between Dental and Orthopaedic Implants: Proceedings of the 3rd Annual Indiana Conference, Indianapolis, Indiana. Indianapolis: Indiana University School of Dentistry; 2002:226-227. 70. Huja SS, Fernandez SA, Hill KJ, Li Y. Remodeling dynamics in the alveolar process in skeletally mature dogs. Anat Rec A Discov Mol Cell Evol Biol 2006;288(12):1243-1249. 71. Garnero P, Szulic DA. Bone remodeling: cellular activities in bone. In: Orwoll ES, Bilezikian JP, Vanderschueren D, eds. Osteoporosis in Men: The Effects of Gender on Skeletal Health. 2nd ed. London: Elsevier; 2010:25-40. 72. Deguchi T, Takano-Yamamoto T, Yabuuchi T, Ando R, Roberts WE, Garetto LP. Histomorphometric evaluation of alveolar bone turnover between the maxilla and the mandible during experimental tooth movement in dogs. Am J Orthod Dentofacial Orthop 2008;133(6):889-897. doi:10.1016/j.ajodo.2006.12.013. 73. Garetto LP, Chen J, Parr JA, Roberts WE. Remodeling dynamics of bone supporting rigidly fixed titanium implants: a histomorphometric comparison in four species including humans. Implant Dent 1995;4(4):235-243. 74. Chen J, Chen K, Garetto LP, Roberts WE. Mechanical response to functional and therapeutic loading of a retromolar endosseous implant used for orthodontic anchorage to mesially translate mandibular molars. Implant Dent 1995;4(4):246-258. 75. Huja SS, Katona TR, Moore BK, Roberts WE. Microhardness and anisotropy of the vital osseous interface and endosseous implant supporting bone. J Orthop Res 1998;16(1):54-60. 76. Cunningham CA, Black SM. Anticipating bipedalism: trabecular organization in the newborn ilium (published online ahead of print May 22, 2009). J Anat 2009;214(6):817-829. doi:10.1111/j.1469-7580. 2009.01073.x. 77. Cunningham CA, Black SM. The neonatal ilium: metaphyseal drivers and vascular passengers (published online ahead of print May 17, 2010). Anat Rec (Hoboken) 2010;293(8):1297-1309. doi:10.1002/ ar.21182. 78. Tanck E, Homminga J, van Lenthe GH, Huiskes R. Increase in bone volume fraction precedes architectural adaptation in growing bone. Bone 2001;28(6):650-654. 79. Abel R, Macho GA. Ontogenetic changes in the internal and external morphology of the ilium in modern humans (published online ahead of print Feb. 17, 2011). J Anat 2011;218(3):324-335. doi:10.1111/ j.1469-7580.2011.01342.x. 80. Christen P, van Rietbergen B, Lambers FM, Müller R, Ito K. Bone morphology allows estimation of loading history in a murine model of bone adaptation (published online ahead of print July 7, 2011). Biomech Model Mechanobiol 2012;11(3-4):483-492. doi:10.1007/ s10237-011-0327-x. 81. Ding M, Odgaard A, Danielsen CC, Hvid I. Mutual associations among microstructural, physical and mechanical properties of human cancellous bone. J Bone Joint Surg Br 2002;84(6):900-907.
April 2013
Copyright © 2013 American Dental Association. All Rights Reserved.