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In vivo measurement of bone deformations using strain gauges

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Abstract

Quantifying the mechanical input to bone is an important step in understanding the form and function of the skeleton. The forces applied to bone at the organ level must be translated to the cellular level and in some way play a role in the maintenance and adaptation of bone tissue. Determining the deformations that a bone normally experiences should help elucidate this mechanotransduction mechanism in bone. To date, the strain gauge, a device that measures the deformations of the material to which it is attached, has been the method used to quantify in vivo bone strains. While the strain gauge suffers from limitations, especially when used in the harsh environment of the body, this device has provided many useful measurements of bone deformations. This chapter covers the development of strain gauges for use with bone and tabulates the in vivo strain measurements recorded over the years to quantify the mechanical loading environment of the skeleton. While strain gauges have been used for many applications using in vitro bone specimens and human cadavers, this chapter will focus on the use of strain gauges to measure in vivo bone strains.
... Thus, strains are measured in vivo by bonding electrical strain gauges to the bone surface with cyanocrylate adhesives. This technique is considered the gold-standard for this purpose (Fritton and Rubin, 2001) and has been validated ex vivo, by confirming excellent correlation (within 2%) between strain recordings obtained simultaneously from such strain gauges bonded to the surface and from optical extensometers (Baggott and Lanyon, 1977;Carter et al., 1980). Since the first in vivo report of this technique in sheep in 1969, (Lanyon and Smith, 1969) it has been used widely to determine in vivo peak strain rates and magnitudes in a large variety of vertebrates (Rubin and Lanyon, 1984b;Fritton and Rubin, 2001). ...
... This technique is considered the gold-standard for this purpose (Fritton and Rubin, 2001) and has been validated ex vivo, by confirming excellent correlation (within 2%) between strain recordings obtained simultaneously from such strain gauges bonded to the surface and from optical extensometers (Baggott and Lanyon, 1977;Carter et al., 1980). Since the first in vivo report of this technique in sheep in 1969, (Lanyon and Smith, 1969) it has been used widely to determine in vivo peak strain rates and magnitudes in a large variety of vertebrates (Rubin and Lanyon, 1984b;Fritton and Rubin, 2001). These techniques will be visited in this thesis to help develop a model of in vivo loading of the murine tibia. ...
... Adaptive morphological variations may be more strongly influenced by strains produced by habitual physiological bending, rather than less-frequent peak or yield strains as suggested by the uniform-safety-factor hypothesis. Experimental studies have demonstrated that limb bone diaphyses of terrestrial animals typically receive spatially and temporally consistent strain distributions during controlled, gait-related activities Biewener, 1993;Fritton and Rubin, 2001). In nearly all limb bone diaphyses that have been studied, the percentage of total normal strain due to bending (hence tension and compression strains) exceeds 70% of the longitudinal strains experienced by a diaphyseal region (Rubin, 1984;Fritton and Rubin, 2001). ...
... Experimental studies have demonstrated that limb bone diaphyses of terrestrial animals typically receive spatially and temporally consistent strain distributions during controlled, gait-related activities Biewener, 1993;Fritton and Rubin, 2001). In nearly all limb bone diaphyses that have been studied, the percentage of total normal strain due to bending (hence tension and compression strains) exceeds 70% of the longitudinal strains experienced by a diaphyseal region (Rubin, 1984;Fritton and Rubin, 2001). Additionally, peak in vivo tensile strains on limb bone diaphyses are typically 70-85% as large as peak compressive strains (Biewener and Taylor, 1986;Biewener, 1993). ...
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It has been hypothesized that a major objective of morphological adaptation in limb-bone diaphyses is the achievement of uniform regional safety factors between discrete cortical locations (e.g. between cranial and caudal cortices at mid-diaphysis). This hypothesis has been tested, and appears to be supported in the diaphyses of ovine and equine radii. The present study more rigorously examined this question using the equine third metacarpal (MC3), which has had functionally generated intracortical strains estimated by a sophisticated finite element model. Mechanical properties of multiple mid-diaphyseal specimens were evaluated in both tension and compression, allowing for testing of habitually tensed or compressed regions in their respective habitual loading mode (`strain-mode-specific' loading). Elastic modulus, and yield and ultimate strength and strain, were correlated with in vivo strain data from a previously published finite element model. Mechanical tests revealed minor variations in elastic modulus, and yield and ultimate strength in both tension and compression loading, while physiological strains varied significantly between the cortices. Contrary to the hypothesis of uniform safety factors, the MC3 has a broad range of tension (caudo-medial, 4.0; cranio-lateral, 37.7) and compression (caudo-medial, 5.7; cranio-lateral, 68.9) safety factors.
... 24 The engendered average strain rate was >30 000 με/s, which is equivalent to physiological strain rates. 25 ...
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The benefits of increased human lifespan depend upon duration of healthy, independent living; the healthspan. Bone‐wasting disorders contribute significantly to loss of independence, frailty, and morbidity in older people. Therefore, there is an unmet need globally for lifestyle interventions to reduce the likelihood of bone fractures with age. Although many mechanisms are involved in disorders of bone loss, there is no single regulatory pathway and, therefore, there is no single treatment available to prevent their occurrence. Our aim in these studies was to determine whether fasting/feeding interventions alter the effect of mechanical loading on bone anabolic activities and increase bone mass. In young 17‐week‐old mice, 16‐hour fasting period followed by reintroduction of food for 2 hours increased markedly the potency of mechanical loading, that mimics the effect of exercise, to induce new cortical bone formation. Consistent with this finding, fasting and re‐feeding increased the response of bone to a loading stimulus that, alone, does not stimulate new bone formation in ad‐lib fed mice. Older mice (20 months) experienced no potentiation of loading‐induced bone formation with the same timing of feeding interventions. Interestingly, the pre‐, prandial, and postprandial endocrine responses in older mice were different from those in young animals. The hormones that change in response to timing of feeding have osteogenic effects that interact with loading‐mediated effects. Our findings indicate associations between timing of food ingestion and bone adaptation to loading. If translated to humans, such non‐pharmacological lifestyle interventions may benefit skeletal health of humans throughout life‐course and in older age.
... A non-invasive servo hydraulic loading machine applied 40 cycles of intermittent loading, with each cycle consisting of: (i) 0.5 N static preload, (ii) 500 N/s ramp up to target peak load, (iii) a 0.05 second hold at peak load, (iv) −500 N/s ramp down to static preload, (v) 10 s rest interval. This has been shown to significantly stimulate loading-related bone gain (Rubin and Lanyon, 1984;Fritton and Rubin, 2001;Robling et al., 2001;Srinivasan et al., 2002;De Souza et al., 2005;Sugiyama et al., 2010Sugiyama et al., , 2011Moustafa et al., 2012). The left tibia of each mouse was used as contralateral control (Sugiyama et al., 2010;McKenzie and Silva, 2011). ...
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The aim of the current study was to quantify the local effect of mechanical loading on cortical bone formation response at the periosteal surface using previously obtained μCT data from a mouse tibia mechanical loading study. A novel image analysis algorithm was developed to quantify local cortical thickness changes (ΔCt.Th) along the periosteal surface due to different peak loads (0N ≤ F ≤ 12N) applied to right-neurectomised mature female C57BL/6 mice. Furthermore, beam analysis was performed to analyse the local strain distribution including regions of tensile, compressive, and low strain magnitudes. Student’s paired t -test showed that ΔCt.Th in the proximal (25%), proximal/middle (37%), and middle (50%) cross-sections (along the z-axis of tibia) is strongly associated with the peak applied loads. These changes are significant in a majority of periosteal positions, in particular those experiencing high compressive or tensile strains. No association between F and ΔCt.Th was found in regions around the neutral axis. For the most distal cross-section (75%), the association of loading magnitude and ΔCt.Th was not as pronounced as the more proximal cross-sections. Also, bone formation responses along the periosteum did not occur in regions of highest compressive and tensile strains predicted by beam theory. This could be due to complex experimental loading conditions which were not explicitly accounted for in the mechanical analysis. Our results show that the bone formation response depends on the load magnitude and the periosteal position. Bone resorption due to the neurectomy of the loaded tibia occurs throughout the entire cross-sectional region for all investigated cortical sections 25, 37, 50, and 75%. For peak applied loads higher than 4 N, compressive and tensile regions show bone formation; however, regions around the neutral axis show constant resorption. The 50% cross-section showed the most regular ΔCt.Th response with increased loading when compared to 25 and 37% cross-sections. Relative thickness gains of approximately 70, 60, and 55% were observed for F = 12 N in the 25, 37, and 50% cross-sections. ΔCt.Th at selected points of the periosteum follow a linear response with increased peak load; no lazy zone was observed at these positions.
... Previous in vivo studies demonstrated that −1000 to −2500 με corresponds to physiological strain levels experienced during walking and other daily activities; however, compressive strains as high as 3000 to 5000 με have been measured during high intensity activities [2,[68][69][70]. In these studies, strain was measured in vivo from strain gauges fixed to the outer surface of the cortex during physiological activities. ...
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Increased bone formation resulting from mechanical loading is well documented; however, the interactions of the mechanotransduction pathways are less well understood. Endothelin-1, a ubiquitous autocrine/paracrine signaling molecule promotes osteogenesis in metastatic disease. In the present study, it was hypothesized that exposure to big endothelin-1 (big ET1) and/or mechanical loading would promote osteogenesis in ex vivo trabecular bone cores. In a 2×2 factorial trial of daily mechanical loading (-2000 με, 120cycles daily, "jump" waveform) and big ET1 (25ng/mL), 48 bovine sternal trabecular bone cores were maintained in bioreactor chambers for 23days. The bone cores' response to the treatment stimuli was assessed with percent change in core apparent elastic modulus (ΔEapp), static and dynamic histomorphometry, and prostaglandin E2 (PGE2) secretion. Two-way ANOVA with a post hoc Fisher's LSD test found no significant treatment effects on ΔEapp (p=0.25 and 0.51 for load and big ET1, respectively). The ΔEapp in the "no load + big ET1" (CE, 13±12.2%, p=0.56), "load + no big ET1" (LC, 17±3.9%, p=0.14) and "load + big ET1" (LE, 19±4.2%, p=0.13) treatment groups were not statistically different than the control group (CC, 3.3%±8.6%). Mineralizing surface (MS/BS), mineral apposition (MAR) and bone formation rates (BFR/BS) were significantly greater in LE than CC (p=0.037, 0.0040 and 0.019, respectively). While the histological bone formation markers in LC trended to be greater than CC (p=0.055, 0.11 and 0.074, respectively) there was no difference between CE and CC (p=0.61, 0.50 and 0.72, respectively). Cores in LE and LC had more than 50% greater MS/BS (p=0.037, p=0.055 respectively) and MAR (p=0.0040, p=0.11 respectively) than CC. The BFR/BS was more than two times greater in LE (p=0.019) and LC (p=0.074) than CC. The PGE2 levels were elevated at 8days post-osteotomy in all groups and the treatment groups remained elevated compared to the CC group on days 15, 19 and 23. The data suggest that combined exposure to big ET1 and mechanical loading results in increased osteogenesis as measured in biomechanical, histomorphometric and biochemical responses.
... Ainsi, seulement les sports "à impact", c'est-à-dire ceux dans lesquels des ha/bf sont présentent (Fritton and Rubin, 2001;Granhed et al., 1987), permettent un gain osseux, si toutefois la pratique de l'activité physique est soutenue dans le temps (Nordstrom et al., 2005). ...
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Bone cells interact in vivo with extracellular matrices mainly formed of type-I collagen, for which the mineral content changes during the bone remodeling cycle. Bone mineral, which is apatitic in nature, was shown to respectively increase and alter the activity and form of osteoblasts. In order to study the micro-environmental effects of the matrix on the preliminary steps of bone formation, it was hypothesized that these morphological alterations could explain the increased activity of the osteoblastic cells by enhancing their mecano-sensibility. This altered mechano-sensibility could in turn modify the osteoblastic cells' response to the widely perceived micro-vibrations in vivo. It was demonstrated that, on the collagen-mineralized materials ACC (Apatite Collagen Complex), MC3T3-E1 pre-osteoblastic cells formed a matrix rich in osteopontin, fibronectin and angiogenic factors. At the same time, an increase in cell adhesion and migration dependent on the mineral content was seen. We also observed an enhanced mechano-sensibility (increased focal adhesion gene expression and turn-over) when cells were cultured on ACC. Furthermore, it was found that the vibratory stimuli response was up-regulated on non-mineralized materials (information) and downregulated on ACC (stress) vs. non-stimulated substrates. This observation was interpreted as a hypersensitization to environmental cues on ACC. Taken together, these data have demonstrated that pre-osteoblastic cell mechanic alterations on ACC give rise to a specific functionalization mimicking what is observed in vivo in the cement line required for bone-formation. ACC-related mechano-sensibility changes, which render ACC a mechanomimetic substrate and lead us to compare the observed cell behavior with osteocytes, could explain the specific matrix deposition and altered response to vibrations. The final goal of establishing a model for in vitro bone remodeling can only be fulfill by considering physico-chemical parameters of the bonematrix and cocultures
Chapter
The conceptual model of the mechanostat proposed by Harold Frost in 1983 is among the most significant contributions to musculoskeletal research today. This model states that bone and other musculoskeletal tissues including cartilage, tendon and muscle respond to habitual exercise/loading and that changes in the loading environment lead to adequate structural adaptation of (bone) tissue architecture. The analogy with a thermostat clearly indicates presence of a physiological feedback system which is able to adjust bone mass and structure according to the engendered loads. In the bioengineering community, the mechanostat has been mathematically formulated as a feedback algorithm using a set point criterion based on a particular mechanical quantity such as strain, strain energy density among others. As pointed out by Lanyon and Skerry, while it is widely thought that in a single individual, there exists a single mechanostat set point, this view is flawed by the fact that different bones throughout the skeleton require a specific strain magnitude to maintain bone mass. Consequently, different bones respond differently to increases or decreases in loading depending on the sensitivity of the mechanostat. Osteocytes, i.e., cells embedded in the bone matrix are believed to be the major bone cells involved in sensing and transduction of mechanical loads. The purpose of this chapter is to review the concept of the mechanostat and its role in bone pathophysiology. To do this we provide examples of why and how the skeleton responds to complex loading stimuli made up of numerous different parameters including strain magnitude, frequency and rest intervals among others. We describe latest in vivo and ex vivo loading models, which allow exploration of various mechanobiological relations in the mechanostat model utilising controlled mechanical environments. A review of the bone cells and signalling transduction cascades involved in mechanosensation and bone adaptation will also be provided. Furthermore, we will discuss the mechanostat in a clinical context, e.g., how factors such as sex, age, genetic constitution, concomitant disease, nutrient availability, and exposure to drugs all affect bone’s response to mechanical loading. Understanding the mechanostat and mechanobiological regulatory factors involved in mechanosensation and desensitisation is essential for our ability to control bone mass based on physiological loading, either directly through different exercise regimens, or by manipulating bone cells in a targeted manner using tailored site and individual specific stimuli including pharmaceuticals.
Article
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Chapter
Growth and remodeling of skeletal tissue in response to its mechanical environment is a well established phenomenon. Relatively little is known regarding the interaction of aging and skeletal responses to mechanical loading, although several early studies have contributed to the “conventional wisdom” that old bones are relatively unresponsive. Development of non-pharmacological therapies for treatment of skeletal pathologies requires better understanding of such interactions, especially if aimed at maintaining or restoring bone mass in the elderly. The use of intrinsic (e.g., running) and extrinsic (e.g., tibial compression) loading models provide means to study age effects in animal studies. We identified 15 studies that address age effects explicitly, although only nine of these include a truly old group (e.g., 18–24 months old for mice). Though the outcomes of the studies have not been uniform, two general themes have emerged. First, bones from old animals are mechano-responsive provided they are presented with an appropriate stimulus. Second, it is unclear if bones from old animals are less responsive than from younger animals, as there is evidence for and against this view. Therefore, we advocate a re-examination of the conventional wisdom, and offer a few guidelines for designing studies to address the questions regarding aging and bone mechano-responsiveness.
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Rosette strain gage, electromyography (EMG), and cineradiographic techniques were used to analyze loading patterns and jaw movements during mastication in Macaca fascicularis. The cineradiographic data indicate that macaques generally swallow frequently throughout a chewing sequence, and these swallows are intercalated into a chewing cycle towards the end of a power stroke. The bone strain and jaw movement data indicate that during vigorous mastication the transition between fast close and the power stroke is correlated with a sharp increase in masticatory force, and they also show that in most instances the jaws of macaques are maximally loaded prior to maximum intercuspation, i.e. during phase I (buccal phase) occlusal movements. Moreover, these data indicate that loads during phase II (lingual phase) occlusal movements are ordinarily relatively small. The bone strain data also suggest that the duration of unloading of the jaw during the power stroke of mastication is largely a function of the relaxation time of the jaw adductors. This interpretation is based on the finding that the duration from 100% peak strain to 50% peak strain during unloading closely approximates the halfrelaxation time of whole adductor jaw muscles of macaques.
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In order to verify the existence of tension and compression forces from the cortical surface of canine femora, rosette strain gauges and a radio telemetry system were used to observe the animals during normal locomotion. Surface strain measured from the lateral cortical surface was consistently in tension whereas surface strain measured from the medical cortical surface was in compression. This data supported in vitro work which showed that eccentric loading of bone results in the convex side of bone being in tension and the concave side of bone being in compression.Spannungs- und Druckkrfte auf der kortikalen Oberflche des Femurs beim Hund wurden geprft. Um die Verhltnisse beim freien Bewegungsablauf beobachten zu knnen, wurden Rosetten-Belastungsmegerte und ein drahtloses Telemetriesystem verwendet. Die abgeleiteten Belastungsmessungen ergaben, da die laterale Kortexoberflche regelmdig unter Spannung stand, whrend die mediale Kortexoberflche unter Druck stand. Dieses Ergebnis besttigt das in vitro Resultat, welches zeigte, da exzentrisches Belasten von Knochen zu Spannung in der konvexen Seite und Druck in der konkaven Seite des Knochens fhrt.
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In order to successfully use strain gages to monitor the mechanical response of biological systems to mechanical inputs, new techniques have been developed. Special procedures for wiring, bonding and waterpooofing strain gages are illustrated. These may change with the type of biological specimen being studied—living or dead—the length of time the gages must function, and the depth of the desired point of application below the surface of the body. Strain gages have been successfully applied deep into the thoracic cavity of a cadaver and have remained operable for a month which is well beyond the required time. Gages applied to the rib cage and the facial bones have been used over a two-month period with no loss in function. For animal tests, applications of up to three weeks are possible with longer periods available with more involved techniques. Strain gages have a distinct advantage over any other type of measuring device which might be employed in that a correlation between static and dynamic results can be determined; this makes it a most useful and valuable tool for the investigator in biomechanics.
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Bone loading was quantified, usingin vivo strain recordings, in the tibiotarsus of growing chicks at 4,8, 12, and 17 weeks of age. The animals were exercised on a treadmil at 35% of their maximum running speed for 15 minutes/day.In vivo bone strains were recorded at six sites on the tibiotarsus. Percentages of the bone's length and a percentage of top running speed were used to define functionally equivalent sites on the bone, and a consistent exercise level over the period of growth was studied. The pattern of bone strain defined in terms of strain magnitude, sign, and orientation remained unchanged from 4–17 weeks of age, a period when bone mass and length increased 10-fold and threefold, respectively. Our findings support the hypothesis that bones model (and remodel) during growth to achieve and maintain a similar distribution of dynamic strains at functionally equivalent sites. Because strain magnitude and sign (tensile versus compressive) differed among recording sites, these data also suggest that cellular responses to strain-mediated stimuli differ from site to site within a bone.
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Two conflicting theories exist concerning the stress pattern for the proximal lateral aspect of the human femur. According to the classic theory of Pauwels, a bending moment on the femur leads to compression medially and to tension laterally. The alternative theory is that muscle forces contribute to a moment-free loading of the femur, with both the medial and lateral cortices subjected to compression. To examine these theories, we measured the strain at the external surface of the proximal lateral aspect of the femur of two female patients undergoing surgery for "snapping hip syndrome." During the surgical procedure, a strain-gauge rosette was bonded to the lateral aspect of the femur and the cortical strains were monitored while the patient performed a series of activities. In both patients, principle tensile strain increased significantly during one-legged stance, walking, and stair climbing as compared with that during two-legged stance. During each loading situation, the principal tensile strain was aligned within 22 degrees to the longitudinal femoral axis. Dynamic strain measurements consistently revealed tensile axial strain at the lateral aspect of the femur during each activity. The present study supports the classic bending theory of Pauwels and demonstrates that the proximal lateral aspect of the femur is subjected to tension during the stance phase of gait.