J Appl Physiol 101: 1113-1117, 2006.
First published May 25, 2006; doi:10.1152/japplphysiol.00612.2005
8750-7587/06 $8.00
Regional variation of tibialis anterior tendon mechanics is lost following denervation
Ellen M. Arruda,1,2
Sarah Calve,2
Robert G. Dennis,3
Kevin Mundy,1 and
Keith Baar4
1Department of Mechanical Engineering and 2Program in Macromolecular Science and Engineering, University of Michigan, Ann Arbor, Michigan; 3Department of Biomedical Engineering, University of North Carolina, Chapel Hill, North Carolina; and 4Division of Molecular Physiology, University of Dundee, Dundee, United Kingdom
Submitted 24 May 2005
; accepted in final form 18 May 2006
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ABSTRACT
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Denervation or inactivity is known to decrease the mass and alter the phenotype of muscle. The mechanical response of tendon to inactivity that has been determined experimentally differs from what is reported by patients. We investigated the hypothesis that this difference was the result of artifacts of the testing process and did not represent what occurred in vivo. To test this hypothesis, a novel approach was used to determine the mechanical properties of the tibialis anterior (TA) tendon by optically measuring the end-to-end mechanical strains as well as the local strains at specific regions of excised TA tendon units. When the end-to-end strain of normal TA tendon is determined, stress-strain response curves show considerably more extensibility than when strain is measured across only the midsection of the tendon (mid-tendon). The strain experienced by the region close to the muscle (muscle tendon) is five times greater than the strain in either the mid-tendon or near the bone (bone-tendon). Five weeks of denervation decreased muscle mass by 67%; increased tendon mass by 10%; and changed the entire shape of the nonlinear response curve, including a loss in regional variation in strain, a 3.9-fold increase in end-to-end tangent modulus, and a 70% reduction in the toe region, as a result of a drastic reduction of the extensibility in the muscle-tendon region. The stress-strain response in the mid-tendon region of a normal TA tendon is therefore not indicative of its overall ability to deform in vivo as it transmits forces from muscle to bone.
mechanics; regional variability; optical stress-strain; inactivity; tendon rupture
TENDONS FUNCTION TO TRANSMIT forces produced by muscle to bone, resulting in movement. Although this basic principle of tendon function has been known for centuries, few seem to appreciate the complexity of this role. Muscle and bone are mechanically divergent tissues. Muscle is highly extensible and compliant, whereas bone is several orders of magnitude more stiff. The tendon is crucial for reducing the impedance mismatch between the compliant muscle tissue and the stiff bone. This fundamental mechanical role of tendon is largely unstudied, and little data exist describing how tendon can transmit forces with high fidelity between two such mechanically different tissues.
Until recently, the stress-strain response of tendons has been determined using grip-to-grip measurements that contain many artifacts of the test apparatus and specimen that affect the measured moduli and failure strains (9). Optical measurement of actual tissue strain has provided a powerful tool for better understanding the mechanical properties of tendon (9, 10, 14, 22). Optical techniques, however, can potentially produce other artifacts if the measurements of tendon mechanics are not made at constant rate of strain or if only a short piece of the entire tendon is used. When Woo and his colleagues (21) gripped the bones on either side of the medial collateral ligament and determined optical stress-strain of the entire ligament, they noted a difference in mechanics depending on whether they measured at the femoral or the tibial end. This suggests that the mechanics of a ligament vary regionally. Whether the same is true for tendon has yet to be determined.
Periods of inactivity have been experimentally shown to decrease the stiffness of tendon (1, 8, 10, 12, 15, 18). This is contrary to some in vivo reports (19) and to what is reported in humans following inactivity in which stiffness is thought to increase, resulting in decreased range of motion (2). We hypothesized that the difference between what patients have reported and what has been experimentally determined by directly measuring the stress-strain characteristics of tendon was due to technical errors introduced when measuring tendon mechanics. To test this hypothesis, we experimentally denervated the right leg of rats for 5 wk and compared the ex vivo mechanics of the entire TA tendon unit (muscle-tendon-bone) from the denervated leg with those of the contralateral control leg. Specific attention was paid to measurement of actual local tissue strains and the differences between strains across the entire length of tendon vs. those across various regions of the tendon.
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METHODS
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Animals.
Four 6-mo-old male Fisher rats were obtained from Charles River Laboratories (Wilmington, MA) and housed in a specific-pathogen-free barrier facility in the Unit for Laboratory Animal Medicine at the University of Michigan until experimentation. After denervation, the rats were housed in a separate specific-pathogen-free return room. All experimental procedures were approved by the University Committee for the Use and Care of Animals at the University of Michigan.
Functional denervation and collection.
Rats were anesthetized with an intraperitoneal injection of pentobarbital sodium (50 mg/kg, supplemented as necessary). The right sciatic nerve, which innervates the muscles of the distal hindlimb, including the tibialis anterior (TA), was exposed before its point of trifurcation, and a 0.5-cm piece was removed (7). The connective tissue and skin were sutured independently, and on recovery the animals were returned to their cages for 5 wk. Five weeks was chosen because the force produced by the muscle decreases to 10% of control value by this time (5).
Determination of tendon strain, tendon stress, nominal stress vs. nominal strain response curve, and tangent stiffness.
To determine the effects of denervation on tendon function, the TA tendon unit (TA muscle, TA tendon, and the 5th metatarsal) was removed from the denervated (n = 4) and contralateral control (n = 3) legs (1 control tendon was transected during isolation) of Fisher rats and stored in sterile PBS before determination of the stress vs. strain response curve. The TA tendon was chosen because it has a long gauge length that is quite uniform in diameter and has a very small aponeurosis (Fig. 1). Higher stress tendons such as the Achilles may have slightly different mechanical properties, but their shorter gauge length and varied diameter make the determination of both local and average stress-strain responses difficult. The stress vs. strain response was determined by placing the TA tendon unit into a bath containing PBS, the muscle and bone were placed into custom grips that resemble alligator clips mounted to hexagonal-shaped stages, and the cross-sectional area (CSA) of the tendon was determined by measuring the diameter at three 60° orientations, fitting an ellipse, and using the ellipse area as the section area. The optical stress-strain device consisted of an optical force transducer with a force resolution of 0.2–200 mN (6), two uniaxial servomotors controlled using the LabVIEW data acquisition system, and a Basler digital video camera connected to a Nikon (model SMZ800) dissecting microscope. The entire TA tendon unit was kept intact and gripped at the bone and muscle; the tendon itself was free standing and immersed in saline (Fig. 1). The tendon length was marked at nine periodic intervals with tissue-marking dye, and the marks were numbered consecutively from left to right. Three sublengths of three marks each were designated and used to measure the local tendon strain as follows: 1–3, muscle-tendon; 4–6, mid-tendon; 7–9, bone-tendon. The average or end-to-end response was measured using ink marks 1 and 9. The samples were loaded at a constant strain rate of 0.01/s without preconditioning until failure, and the synchronized force and image recordings were compiled using LabVIEW. The raw load data were converted to nominal stress by dividing the load by the sublength CSA of the tendon, and the image data were converted to nominal strain by optically determining the change in separation of ink marks and dividing this number by the initial separation of ink marks. The maximum tangent stiffness is defined as the maximum slope of a nonlinear stress-strain response curve. The stress-strain response curves for the tendons were initially nonlinear in the toe region and became linear at larger strains. The maximum tangent stiffness was calculated as the slope of the stress-strain curve in the linear region.
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Fig. 1. Mechanical testing of tibialis anterior tendon unit using optical stress-strain device. The tibialis anterior tendon unit was gripped at the muscle (left) and the 5th metatarsal (right), cross-sectional area was determined, and 9 marks were made on the tendon with tissue marking dye. The marks were numbered consecutively from left to right and used to measure the local tendon strain as follows: 1–3, muscle-tendon; 4–6, mid-tendon; 7–9, bone-tendon. The end-to-end response is measured using ink marks 1–9.
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Determination of collagen concentration and content.
The TA tendon and TA muscles were surgically removed from the denervated and contralateral control legs 5 wk following denervation. The tendons and muscles were stripped of overlying connective tissue and fat and placed in sterile PBS before the determination of hydroxyproline using the method of Woessner (20). Briefly, tendons and muscles were dried at 110°C for 1 h and weighed immediately. The tissue was then digested overnight in 6 N hydrochloric acid at 130°C. The next day the pH was raised to 
7 by addition of sodium hydroxide, chloramine T was added, and the tubes were incubated for 20 min at room temperature. The chloramine T was inactivated by the addition of perchloric acid before an equal volume of Ehrlich's reagent was added. The tubes were incubated at 60°C for 20 min, cooled, and absorbance measured at 557 nm. Hydroxyproline was converted to collagen assuming that it accounts for 13.8% of the total collagen as suggested by Neuman and Logan (16). Collagen concentration was determined by normalizing the collagen content to the dry mass of the tissue.
Statistics.
Data are presented as means ± SE for three to four tendons per group. Differences in mean values were compared within groups (e.g., control vs. denervated), and significant differences were determined by Student's t-test. The level of significance was set at P < 0.05.
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RESULTS
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Regional differences in normal tendon function.
The TA tendon unit was removed, and the nominal stress vs. nominal strain relationship was determined optically for both the entire tendon length (the average or end-to-end response) and for subregions along the tendon length (Fig. 1). Tendon failure during the test occurred predominantly within the bulk of the tendon and not at either the myotendinous junction or enthesis. Normal tendon is functionally graded (Fig. 2); its mechanical response curve varies along its length. At the region near the bone (bone-tendon), the maximum tangent modulus of the tendon was 2.1-fold higher than that of either the midsection (mid-tendon) or the tendon near the muscle (muscle-tendon). Also, the extensibility of the muscle-tendon region greatly exceeds that of the other two regions; at any given stress level the strain in the muscle-tendon region was at least fives times greater than the mid-tendon or bone-tendon strains (Fig. 2).
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Fig. 2. Regional differences exist in the elasticity and stiffness of normal tendon. The tibialis anterior tendon unit from the control leg of Fisher rats was mechanically tested and regionally analyzed. The tibialis anterior tendon stress-strain response in the region of the tendon near the bone (bone-tendon, curve 1), the midsection (mid-tendon, curve 2), the region of the tendon close to the muscle (muscle-tendon, curve 4), and the average strain measured across the entire tendon and load normalized by the average section cross-sectional area (end-to-end, curve 3) are shown. Normal tendon mechanics are functionally graded with the muscle-tendon region being more extensible and less stiff than the bone-tendon region.
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Effects of denervation on tendon mechanics.
Five weeks of functional denervation resulted in gross changes in the shape of the end-to-end stress-strain response curve of the TA tendon unit (Fig. 3). The initial toe region is truncated and sharply transitions to a high-stiffness regime at strains below 1%. Tendons from the denervated leg had a maximum tangent modulus of 763 ± 265 MPa, whereas those from the contralateral control had a maximum modulus of 195 ± 36 MPa. The increase in tendon stiffness was accompanied by a 70% decrease in extensibility of the toe region. The increase in stiffness and decrease in extensibility were the result of a leftward shift of the strain experienced by the muscle-tendon and mid-tendon regions only (Fig. 4).
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Fig. 3. Five weeks of inactivity decrease tendon compliance and extensibility. The end-to-end nominal stress vs. actual tissue averaged strain for the tibialis anterior tendon from control (n = 3) and denervated (n = 4) legs of Fisher rats. The tibialis anterior tendon was loaded at a constant strain rate until failure, and the synchronized force and image recordings were compiled. The raw load vs. image data were converted to nominal stress (load/cross-sectional area) vs. nominal strain (change in separation of ink marks/initial separation). The (maximum) tangent stiffness was determined by calculating the secondary slope of the nominal stress vs. nominal strain data. The results of all tests are shown to demonstrate the low variability within each group, and they demonstrate the distinct differences between the 2 groups.
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Fig. 4. Decreased extensibility and increased stiffness in the region of tendon proximal to muscle following 5 wk of denervation. Representative traces of the regional stress-strain response of the tibialis anterior tendon unit from the denervated leg of Fisher rats are shown. The tibialis anterior tendon response in the bone-tendon region (curve 1), the mid-tendon region (curve 2), the muscle-tendon region (curve 4), and the end-to-end strain (curve 3) are presented. There is a decrease in the extensibility and an increase in the stiffness of the muscle-tendon region following 5 wk of denervation. Moreover, there is no significant variation in the tendon mechanics along its length.
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Gross characteristics of muscle and tendon following denervation.
Denervation resulted in a 67 ± 2% decrease in the mass of the TA muscle and a 10 ± 3% increase in the mass of the TA tendon, resulting in a 3.61 ± 0.28-fold increase in the tendon-to-muscle ratio (Table 1). The concentration of collagen within the TA muscle increased 2.91 ± 0.39-fold, whereas the overall content of collagen was statistically unchanged. Neither the tendon collagen concentration nor content was significantly changed.
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DISCUSSION
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We have developed a method for determining the actual stress-strain relationship for a tendon unit. Using this method we show that within a single, intact, normal TA tendon unit there are regional mechanical differences with the muscle-tendon region having greater toe region and overall extensibility (strain to failure) and toe region compliance (inverse stiffness or inverse slope) than the bone-tendon region. Inactivity results in decreased end-to-end extensibility of the toe region, decreased end-to-end tendon extensibility (strain to failure) and a 3.9-fold increase in end-to-end stiffness primarily due to changes in the muscle-tendon region.
Haraldsson et al. (9) have previously reported differences in the yield stress and modulus of fascicles from the anterior vs. the posterior of the patellar tendon of humans. However, it is unclear how these differences alter the mechanics of the whole tendon or contribute to the overall mechanical function of the tendon. Lieber and his colleagues (11) noted that in the frog semitendinosis muscle, the aponeurosis was characterized by both a more compliant toe region and a stiffer secondary modulus than either the bone-tendon interface or the tendon itself (11). Their findings demonstrate a trend similar to that reported here, but here the mechanical differences are seen within the tendon itself. Whereas the present study is the first to identify and characterize tendon as a functionally graded structure along its length, others have noted regional differences in crimp (3), glycosaminoglycans (4), and hydroypyridinium cross-linking (4). Of particular interest is the finding of Curwin and colleagues (4) that cross-linking was greater in the bone-tendon region. Because cross-linking of collagen increases tendon stiffness, this may be the underlying mechanism behind the regional mechanical variation that we observed. Together, these findings demonstrate the mechanical complexity of tendons, showing that a single tissue can have more than one mechanical function, allowing it to transmit forces with limited impedance mismatch. Near the interface with the compliant muscle, the tendon is more extensible (the strain is large at a given stress level), whereas near the bone interface the tendon is significantly stiffer (the same applied stress results in less strain).
The majority of previous ex vivo studies of tendon mechanics have severed the tendon from the muscle and bone and examined the response of the mid-tendon region only (1, 8, 12, 22). This technique introduces several sources of error into the measurement. First, cutting tendons disrupts the normal intrafibrillar connections within the organ. Using pieces of tendon cut from the rat tail, we noted that the stress-strain response was variable due to fibril sliding within the tendon that was visible on direct microscopic observation (data not shown). When the whole tendon unit was used, fibril sliding was no longer detectable, and the quantitative variability of the measures commensurately decreased. Another consequence of cutting the tendon and gripping the tendon directly is the introduction of stress or strain concentrations at the ends that can result in premature tearing of the tissue at the grip region that is not consistent with the physiological response (9). Cutting the tendon also tends to render the specimen length-to-diameter ratio too low for a valid uniaxial tension test. When length-to-diameter ratio is less than four, the specimen is typically in a state of plane strain and all stress-strain curves generated and the moduli measured are not true uniaxial deformation values. Most importantly for the present study, a consequence of the functional variation in tendon response is that the mid-tendon response is not indicative of the average end-to-end response in a tendon. Test protocols that examine only the mid-tendon region, even if they are achieved by placing ink marks across this sublength of the tendon and measuring the actual tissue strain locally, will result in stress-strain response curves that have a higher tangent stiffness than the end-to-end tendon response at all strain levels. This is illustrated in Fig. 5 in which two curves from Fig. 2, the local response of the mid-tendon region and the average response of the tendon end-to-end, are replotted as the mid-tendon (CTL) response and the end-to-end (CTL) response, respectively. It is clear that a tangent line drawn to the mid-tendon (CTL) curve at any given strain level will have a higher slope than a tangent line to the end-to-end (CTL) curve at that same strain level. This result demonstrates a critical need to adopt a standardized method for characterizing tendon mechanics because the actual response of the TA tendon is best represented by the end-to-end response curve and not by the mid-tendon curve.
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Fig. 5. Comparison of stress-strain response in the mid-section of the tibialis anterior tendon after 5 wk of denervation. Inconsistencies between our data and that of others can be explained comparing mid-tendon and end-to-end responses of control (CTL) and denervated (DEN) tendon. Moreover, because the denervated tendon is not functionally graded, the mid-tendon and end-to-end response are functionally similar. If comparisons are made between the mid-tendon of the control (solid tangent) and the mid-tendon of the denervated (dotted tangent), the tangent stiffness following 5 wk of denervation appears to decrease. However, if the proper comparison is made [that of end-to-end control (dashed tangent) and the end-to-end denervated] the decreased initial compliance and increased tangent stiffness of the denervated tendon are evident. Representative stress-strain curves for the control mid-tendon (curve 1), denervated end-to-end (curve 2), and control end-to-end (curve 3) regions are shown.
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Following 5 wk of denervation, there was an increase in the end-to-end stiffness of the TA tendon and a complete loss of the regional differences associated with normal tendon. This finding contrasts a number of studies that have shown that inactivity decreases in vitro tendon stiffness (1, 8, 12). However, these studies have all compared, the mid-tendon response curves using cut tendons rather than their end-to-end responses. If only the mid-tendon response curves of control and denervated tendons are compared, the present results are consistent with this literature. In this case, at small strain levels, the denervated response curve would have a lower tangent stiffness (Fig. 5). However, these are not the proper curves to compare. If the end-to-end response of the control and denervated tendon are compared, the denervated tissue has an increased tangent stiffness at all strain levels. This result is also illustrated in Fig. 5 in which the end-to-end response curve for a denervated tendon is plotted (curve 2) along with its corresponding initial tangent stiffness (dotted tangent). As stated previously, at every strain level the slope of a tangent to the denervated curve will exceed that of the end-to-end control curve (curve 3), and therefore the tangent modulus of denervated tissue exceeds that of normal TA tendon. Because the response of the denervated tendon is fairly homogeneous along its length, we can also compare the denervated end-to-end curve with that of the mid-tendon control (curve 1). Doing this would yield the same improper conclusion that previous investigators have made: that the control was stiffer than the denervated.
In vivo measures of human tendon stiffness using MRI images and an external standard have also shown a decrease in tendon stiffness following inactivity (10, 15, 18). An important difference between the ex vivo determination of tendon mechanics described here and the in vivo measures done in humans is that the in vivo measures are made using the individual's own muscle to load the tendon. This results in two important differences compared with the present model. First, in vivo the rate of loading of the tendon changes as the muscle undergoes hypertrophy or atrophy (13). Because tendon is a viscoelastic tissue, changes in the rate of tendon loading result in a change in the measured stress-strain response in the absence of changes in the properties of the tendon. Second, isometric contraction of the associated muscles results in a very small strain on the tendon. As shown in Fig. 5, at very low strains, the mid-tendon region appears to be less stiff following inactivity. When greater strains are applied, equivalent to walking or running, the inactive tendon is much stiffer than the control. This may explain why activities that include large strain-lengthening contractions, such as walking down stairs, are more difficult following a period of inactivity.
In conclusion, using a novel optical method, we have found that the TA tendon normally has varied mechanical properties along its length, allowing it to transfer mechanical force and power from a compliant tissue to a stiff tissue with high fidelity. Inactivity results in a significantly stiffer and less extensible tendon, largely due to the stiffening of the muscular end of the tendon. Because in normal tendon this region may protect muscle from injury, this might explain the increased incidence of muscle injury following reloading after periods of inactivity.
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GRANTS
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This work was supported by United States Defense Advanced Research Projects Agency Navy Grant 66001-02-C-803 and by National Science Foundation, Civil and Mechanical Systems Grant CMS9988693. S. Calve was supported by the University of Michigan GE-Rackham Merit Fellowship.
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FOOTNOTES
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Address for reprint requests and other correspondence: K. Baar, Div. of Molecular Physiology, Univ. of Dundee, MSI/WTB Dow St., Dundee DD1 5EH, UK (e-mail: k.baar{at}dundee.ac.uk)
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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Copyright © 2006 by the American Physiological Society.
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ABSTRACT
METHODS
