Anisotropy of spin relaxation of water protons in cartilage and tendon

Transverse spin relaxation rates of water protons in articular cartilage and tendon depend on the orientation of the tissue relative to the applied static magnetic field. This complicates the interpretation of magnetic resonance images of these tissues. At the same time, relaxation data can provide information about their organisation and microstructure. We present a theoretical analysis of the anisotropy of spin relaxation of water protons observed in fully hydrated cartilage. We demonstrate that the anisotropy of transverse relaxation is due almost entirely to intramolecular dipolar coupling modulated by a specific mode of slow molecular motion: the diffusion of water molecules in the hydration shell of a collagen fibre around the fibre, such that the molecular director remains perpendicular to the fibre. The theoretical anisotropy arising from this mechanism follows the “magic-angle” dependence observed in magnetic-resonance measurements of cartilage and tendon and is in good agreement with the available experimental results. We discuss the implications of the theoretical findings for MRI of ordered collagenous tissues.

Incidental walking activity is sufficient to induce time-dependent conditioning of the Achilles tendon

The Achilles tendon has been seen to exhibit time-dependent conditioning when isometric muscle actions were of a prolonged duration, compared to those involved in dynamic activities, such as walking. Since, the effect of short duration muscle activation associated with dynamic activities is yet to be established, the present study aimed to investigate the effect of incidental walking activity on Achilles tendon diametral strain. Eleven healthy male participants refrained from physical activity in excess of the walking required to carry out necessary daily tasks and wore an activity monitor during the 24 h study period. Achilles tendon diametral strain, 2 cm proximal to the calcaneal insertion, was determined from sagittal sonograms. Baseline sonographic examinations were conducted at ∼08:00 h followed by replicate examinations at 12 and 24 h. Walking activity was measured as either present (1) or absent (0) and a linear weighting function was applied to account for the proximity of walking activity to tendon examination time. Over the course of the day the median (min, max) Achilles tendon diametral strain was −11.4 (4.5, −25.4)%. A statistically significant relationship was evident between walking activity and diametral strain (P < 0.01) and this relationship improved when walking activity was temporally weighted (AIC 131 to 126). The results demonstrate that the short yet repetitive loads generated during activities of daily living, such as walking, are sufficient to induce appreciable time-dependant conditioning of the Achilles tendon. Implications arise for the in vivo measurement of Achilles tendon properties and the rehabilitation of tendinopathy.

Eccentric calf muscle exercise produces a greater acute reduction in Achilles tendon thickness than concentric exercise

Objective: To investigate the acute effects of isolated eccentric and concentric calf muscle exercise on Achilles tendon sagittal thickness. ---------- Design: Within-subject, counterbalanced, mixed design. ---------- Setting: Institutional. ---------- Participants: 11 healthy, recreationally active male adults. ---------- Interventions: Participants performed an exercise protocol, which involved isolated eccentric loading of the Achilles tendon of a single limb and isolated concentric loading of the contralateral, both with the addition of 20% bodyweight. ---------- Main outcome measurements: Sagittal sonograms were acquired prior to, immediately following and 3, 6, 12 and 24 h after exercise. Tendon thickness was measured 2 cm proximal to the superior aspect of the calcaneus. ---------- Results: Both loading conditions resulted in an immediate decrease in normalised Achilles tendon thickness. Eccentric loading induced a significantly greater decrease than concentric loading despite a similar impulse (−0.21 vs −0.05, p<0.05). Post-exercise, eccentrically loaded tendons recovered exponentially, with a recovery time constant of 2.5 h. The same exponential function did not adequately model changes in tendon thickness resulting from concentric loading. Even so, recovery pathways subsequent to the 3 h time point were comparable. Regardless of the exercise protocol, full tendon thickness recovery was not observed until 24 h. ---------- Conclusions: Eccentric loading invokes a greater reduction in Achilles tendon thickness immediately after exercise but appears to recover fully in a similar time frame to concentric loading.

Conditioning of the Achilles tendon via ankle exercise improves correlations between sonographic measures of tendon thickness and body anthropometry

Although conditioning is routinely used in mechanical tests of tendon in vitro, previous in vivo research evaluating the influence of body anthropometry on Achilles tendon thickness has not considered its potential effects on tendon structure. This study evaluated the relationship between Achilles tendon thickness and body anthropometry in healthy adults both before and after resistive ankle plantarflexion exercise. A convenience sample of 30 healthy male adults underwent sonographic examination of the Achilles tendon in addition to standard anthropometric measures of stature and body weight. A 10-5 MHz linear array transducer was used to acquire longitudinal sonograms of the Achilles tendon, 20 mm proximal to the tendon insertion. Participants then completed a series (90-100 repetitions) of conditioning exercises against an effective resistance between 100% and 150% body weight. Longitudinal sonograms were repeated immediately on completion of the exercise intervention, and anteroposterior Achilles tendon thickness was determined. Achilles tendon thickness was significantly reduced immediately following conditioning exercise (t = 9.71, P < 0.001), resulting in an average transverse strain of -18.8%. In contrast to preexercise measures, Achilles tendon thickness was significantly correlated with body weight (r = 0.72, P < 0.001) and to a lesser extent height (r = 0.45, P < 0.01) and body mass index (r = 0.63, P < 0.001) after exercise. Conditioning of the Achilles tendon via resistive ankle exercises induces alterations in tendon structure that substantially improve correlations between Achilles tendon thickness and body anthropometry. It is recommended that conditioning exercises, which standardize the load history of tendon, are employed before measurements of sonographic tendon thickness in vivo.

Measuring mechanical properties of tendon in vivo

Introduction: Understanding the mechanical properties of tendon is an important step to guiding the process of improving athletic performance, predicting injury and treating tendinopathies. The speed of sound in a medium is governed by the bulk modulus and density for fluids and isotropic materials. However, for tendon,which is a structural composite of fluid and collagen, there is some anisotropy requiring an adjustment for Poisson’s ratio. In this paper, these relationships are explored and modelled using data collected, in vivo, on human Achilles tendon. Estimates for elastic modulus and hysteresis based on speed of sound data are then compared against published values from in vitro mechanical tests. Methods: Measurements using clinical ultrasound imaging, inverse dynamics and acoustic transmission techniques were used to determine dimensions, loading conditions and longitudinal speed of sound for the Achilles tendon during a series of isometric plantar flexion exercises against body weight. Upper and lower bounds for speed of sound versus tensile stress in the tendon were then modelled and estimates derived for elastic modulus and hysteresis. Results: Axial speed of sound varied between 1850 to 2090 m.s−1 with a non-linear, asymptotic dependency on the level of tensile stress in the tendon 5–35 MPa. Estimates derived for the elastic modulus ranged between 1–2 GPa. Hysteresis derived from models of the stress-strain relationship, ranged from 3–11%. These values agree closely with those previously reported from direct measurements obtained via in vitro mechanical tensile tests on major weight bearing tendons. Discussion: There is sufficiently good agreement between these indirect (speed of sound derived) and direct (mechanical tensile test derived) measures of tendon mechanical properties to validate the use of this non-invasive acoustic transmission technique. This non-invasive method is suitable for monitoring changes in tendon properties as predictors of athletic performance, injury or therapeutic progression.

Load bearing improves the limits of agreement for repeated in vivo measures of the speed of sound in human Achilles tendon

Axial acoustic wave propagation has been widely used in evaluating the mechanical properties of human bone in vivo. However, application of this technique to monitor soft tissues, such as tendon, has received comparatively little scientific attention. Laboratory-based research has established that axial acoustic wave transmission is not only related to the physical properties of equine tendon but is also proportional to tensile load to which it is exposed (Miles et al., 1996; Pourcelot et al., 2005). The reproducibility of the technique for in vivo measurements in human tendon, however, has not been established. The aim of this study was to evaluate the limits of agreement for repeated measures of the speed of sound (SoS) in human Achilles tendon in vivo. Methods: A custom built ultrasound device, consisting of an A-mode 1MHz emitter and two regularly spaced receivers, was used to measure the SoS in the mid-portion of the Achilles tendon in ten healthy males and ten females (mean age: 33.8 years, range 23-56 yrs; height: 1.73±0.08 m; weight: 68.4±15.3 kg). The emitter and receivers were held at fixed positions by a polyethylene frame and maintained in close contact with the skin overlying the tendon by means of elasticated straps. Repeated SoS measurements were taken with the subject prone (non-weightbearing and relaxed Achilles tendon) and during quiet bipedal and unipedal stance. In each instance, the device was detached and repositioned prior to measurement. Results: Limits of agreement for repeated SoS measures during non-weightbearing and bipedal and unipedal stance were ±53, ±28 and ±21 m/s, respectively. The average SoS in the non-weightbearing Achilles tendon was 1804±198 m/s. There was a significant increase in the average SoS during bilateral (2122±135 m/s) (P < 0.05) and unilateral (2221±79 m/s) stance (P < 0.05). Conclusions: Repeated SoS measures in human Achilles tendon were more reliable during stance than under non-weightbearing conditions. These findings are consistent with previous research in equine tendon in which lower variability in SoS was observed with increasing tensile load (Crevier-Denoix et al, 2009). Since the limits of agreement for Achilles tendon SoS are nearly 5% of the changes previously observed during walking and therapeutic heel raise exercises, acoustic wave transmission provides a promising new non-invasive method for determining tendon properties during sports and rehabilitation related activities.

The acute transverse strain response of the patellar tendon to quadriceps exercise

Introduction: The human patellar tendon is highly adaptive to changes in habitual loading but little is known about its acute mechanical response to exercise. This research evaluated the immediate transverse strain response of the patellar tendon to a bout of resistive quadriceps exercise. Methods: Twelve healthy adult males (mean age 34.0+/-12.1 years, height 1.75+/-0.09 m and weight 76.7+/-12.3 kg) free of knee pain participated in the research. A 10-5 MHz linear-array transducer was used to acquire standardised sagittal sonograms of the right patellar tendon immediately prior to and following 90 repetitions of a double-leg parallel-squat exercise performed against a resistance of 175% bodyweight. Tendon thickness was determined 20-mm distal to the pole of the patellar and transverse Hencky strain was calculated as the natural log of the ratio of post- to pre-exercise tendon thickness and expressed as a percentage. Measures of tendon echotexture (echogenicity and entropy) were also calculated from subsequent gray-scale profiles. Results: Quadriceps exercise resulted in an immediate decrease in patellar tendon thickness (P<.05), equating to a transverse strain of -22.5+/-3.4%, and was accompanied by increased tendon echogenicity (P<.05) and decreased entropy (P<.05). The transverse strain response of the patellar tendon was significantly correlated with both tendon echogenicity (r = -0.58, P<.05) and entropy following exercise (r=0.73, P<.05), while older age was associated with greater entropy of the patellar tendon prior to exercise (r=0.79, P<.05) and a reduced transverse strain response (r=0.61, P<.05) following exercise. Conclusions: This study is the first to show that quadriceps exercise invokes structural alignment and fluid movement within the matrix that are manifest by changes in echotexture and transverse strain in the patellar tendon., (C)2012The American College of Sports Medicine

Overweight and obesity alters the cumulative transverse strain in the Achilles tendon immediately following exercise

This research evaluated the effect of obesity on the acute cumulative transverse strain of the Achilles tendon in response to exercise. Twenty healthy adult males were categorized into ‘low normal-weight’ (BMI <23 kg m−2) and ‘overweight’ (BMI >27.5 kg m−2) groups based on intermediate cut-off points recommended by the World Health Organization. Longitudinal sonograms of the right Achilles tendon were acquired immediately prior and following weight-bearing ankle exercises. Achilles tendon thickness was measured 20-mm proximal to the calcaneal insertion and transverse tendon strain was calculated as the natural log of the ratio of post- to pre-exercise tendon thickness. The Achilles tendon was thicker in the overweight group both prior to (t18 = −2.91, P = 0.009) and following (t18 = −4.87, P < 0.001) exercise. The acute transverse strain response of the Achilles tendon in the overweight group (−10.7 ± 2.5%), however, was almost half that of the ‘low normal-weight’ (−19.5 ± 7.4%) group (t18 = −3.56, P = 0.004). These findings suggest that obesity is associated with structural changes in tendon that impairs intra-tendinous fluid movement in response to load and provides new insights into the link between tendon pathology and overweight and obesity.

The acute response of tendon to loading: implications for rehabilitation

Achilles tendinopathy is a common disorder involving physically active and sedentary individuals alike. Although the processes underlying its development are poorly understood, tendinopathy is widely regarded as an ‘overuse’ injury in which the tendon fails to adapt to prevalent loading conditions. Paradoxically, there is emerging evidence that heavy eccentric loading of the Achilles tendon may be an effective conservative approach for treatment of tendinopathy, with success rates of 60–80% reported. Interestingly, loading exercises involving other forms of muscle action, such as concentric activation, have been shown to be less effective treatment options. However, little is known about the acute response of tendon to exercise at present, and there are few plausible explanatory mechanisms for the observed beneficial effects of eccentric exercise, as opposed to other forms of strain stimuli. This paper presents the findings from a series of experiments undertaken to evaluate the effect of various strain stimuli on the time-dependent response of human Achilles tendon in vivo. It was shown for the first time, that heavy resistive ankle plantarflexion/ dorsiflexion exercises induced an immediate and significant decrease in Achilles tendon thickness (~15%). While thickness returned to pre-exercise levels within 24 hours, the recovery was exponential, with primary recovery occurring in less than 6 hours post-exercise. We proposed that such a diametral strain response with tensile loading reflects collagen realignment, Poison’s effects and radial extrusion of water from the tendon core. With unloading, the recovery of tendon dimensions likely reflects the re-diffusion of water via osmotic and/or inflammatory driven processes. Interestingly, prolonged walking was found to induce a similar diametral strain response. In subsequent studies, we demonstrated that eccentric exercise resulted in a greater reduction (-21%) in Achilles tendon thickness than isolated concentric exercise alone (-5%), despite a similar loading impulse. These novel findings, coupled with observations of a reduced diametral strain response with tendon pathology, highlight the importance of fluid movement to tendon function, nutrition and health. They also provide new insights into potential mechanisms underlying Achilles tendinopathy that impact rehabilitation strategies.

Reproducibility and clinical utility of tendon palpation to detect patellar tendinopathy in young basketball players

Background—Palpation is an important clinical test for jumper's knee. Objectives—To (a) test the reproducibility of palpation tenderness, (b) evaluate the sensitivity and specificity of palpation in subjects with clinical symptoms of jumper's knee, and (c) determine whether tenderness to palpation may serve as a useful screening test for patellar tendinopathy. The yardstick for diagnosis of patellar tendinopathy was ultrasonographic abnormality. Methods—In 326 junior symptomatic and asymptomatic athletes' tendons, palpation was performed by a single examiner before ultrasonographic examination by a certified ultrasound radiologist. In 58 tendons, palpation was performed twice to test reliability. Tenderness to palpation was scored on a scale from 0 to 3 where 0 represented no pain, and 1, 2, and 3 represented mild, moderate, and severe tenderness respectively. Results—Patellar tendon palpation was a reliable examination for a single examiner (Pearson r = 0.82). In symptomatic tendons, the positive predictive value of palpation was 68%. As a screening examination in asymptomatic subjects, the positive predictive value of tendon palpation was 36–38%. Moderate and severe palpation tenderness were better predictors of ultrasonographic tendon pathology than absent or mild tenderness (p<0.001). Tender and symptomatic tendons were more likely to have ultrasound abnormality than tenderness alone (p<0.01). Conclusions—In this age group, palpation is a reliable test but it is not cost effective in detecting patellar tendinopathy in a preparticipation examination. In symptomatic tendons, palpation is a moderately sensitive but not specific test. Mild tenderness in the patellar tendons in asymptomatic jumping athletes should be considered normal.

Patellar tendon ultrasonography in asymptomatic active athletes reveals hypoechoic regions : a study of 320 tendons

OBJECTIVE: To compare patellar tendon sonographic findings in active, currently asymptomatic, elite athletes with those in nonathletic controls. DESIGN: Cross-sectional cohort study with convenience control sample. SETTING: The Victorian Institute of Sport Tendon Study Group, an institutional elite athlete study group in Australia. PATIENTS AND PARTICIPANTS: Two hundred elite male and female athletes from the sports of basketball, cricket, netball, and Australian rules football. Forty athletes who had current symptoms of jumper's knee were excluded from analysis, leaving 320 subject tendons in athletes who were currently asymptomatic. Twenty-seven nonathletic individuals served as controls. MAIN OUTCOME MEASURE: Sonographic patellar tendon appearance. We measured the dimensions of subject tendons and noted the presence or absence of hypoechoic regions and tendon calcification. Dimensions of hypoechoic regions were measured, and approximate cross-sectional areas were calculated. Chi-squared analysis was used to test the prevalence of hypoechoic regions in subjects and controls and men and women. RESULTS: In currently asymptomatic subjects, hypoechoic regions were more prevalent in athlete tendons (22%) than in controls (4%), in male subject tendons (30%) than in female subjects (14%), and in basketball players (32%) than in other athletes (9%) (all p < 0.01). Bilateral tendon abnormalities were equally prevalent in men and women but more prevalent in basketball players (15%) than in other athletes (3%) (p < 0.05). Sonographic hypoechoic regions were present in 35 of 250 (14%) patellar tendons in athletes who had never had anterior knee pain. CONCLUSIONS: Patellar tendon sonographic hypoechoic areas were present in asymptomatic patellar tendons of a proportion of elite athletes but rarely present in controls. This has implications for clinicians managing athletes with anterior knee pain.

Asymptomatic hypoechoic regions on patellar tendon ultrasound : a 4-year clinical and ultrasound followup of 46 tendons

Patellar tendon ultrasound appearance is commonly used in clinical practice to diagnose patellar tendinopathy and guide management. Using a longitudinal study design we examined whether or not the presence of a hypoechoic ultrasonographic lesion in an asymptomatic patellar tendon conferred a risk for developing jumper's knee compared with a tendon that was ultrasonographically normal. Ultrasonographic, symptomatic and anthropometric assessment was completed at baseline and followup. Magnetic resonance imaging was performed on four tendons that resolved ultrasonographically in the study period. Forty-six patellar tendons were followed over 47 ± 11.8 months. Eighteen tendons were hypoechoic at baseline and 28 were ultrasonographically normal. Five tendons resolved ultrasonographically in the study period. Magnetic resonance imaging in four of these tendons was normal. Seven normal patellar tendons at baseline developed a hypoechoic area but only two became symptomatic. Analysis of ultrasonography at baseline and clinical outcome with Fisher's exact test shows there is no association between baseline ultrasound changes and symptoms at followup. In this study there is no statistically significant relationship between ultrasonographic patellar tendon abnormalities and clinical outcome in elite male athletes. Management of jumper's knee should not be solely based on ultrasonographic appearance; clinical assessment remains the cornerstone of appropriate management.

A poly(lactic-co-glycolic acid) knitted scaffold for tendon tissue engineering: an in vitro and in vivo study

We have designed a composite scaffold for potential use in tendon or ligament tissue engineering. The composite scaffold was made of a cellularized alginate gel that encapsulated a knitted structure. Our hypothesis was that the alginate would act as a cell carrier and deliver cells to the injury site while the knitted structure would provide mechanical strength to the composite construct. The mechanical behaviour and the degradation profile of the poly(lactic-co-glycolic acid) knitted scaffolds were evaluated. We found that our scaffolds had an elastic modulus of 750 MPa and that they lost their physical integrity within 7 weeks of in vitro incubation. Autologous rabbit mesenchymal stem cell seeded composite scaffolds were implanted in a 1-cm-long defect created in the rabbit tendon, and the biomechanical properties and the morphology of the regenerated tissues were evaluated after 13 weeks. The regenerated tendons presented higher normalized elastic modulus of (60%) when compared with naturally healed tendons (40%). The histological study showed a higher cell density and vascularization in the regenerated tendons.

Non-invasive clinical measurement of the viscoelastic properties of tendon using acoustic wave transmission

Background. In isotropic materials, the speed of acoustic wave propagation is governed by the bulk modulus and density. For tendon, which is a structural composite of fluid and collagen, however, there is some anisotropy requiring an adjustment for Poisson's ratio. This paper explores these relationships using data collected, in vivo, on human Achilles tendon and then compares estimates of elastic modulus and hysteresis against published values from in vitro mechanical tests. Methods. Measurements using conventional B-model ultrasound imaging, inverse dynamics and acoustic transmission techniques were used to determine dimensions, loading conditions and longitudinal speed of sound in the Achilles tendon during a series of isometric plantar flexion exercises against body weight. Upper and lower bounds for speed of sound versus tensile stress in the tendon were then modelled and estimates of the elastic modulus and hysteresis of the Achilles tendon derived. Results. Axial speed of sound varied between 1850 and 2090 ms-1 with a non-linear, asymptotic dependency on the level of tensile stress (5-35 MPa) in the tendon. Estimates derived for the elastic modulus of the Achilles tendon ranged between 1-2 GPa. Hysteresis derived from models of the stress-strain relationship, ranged from 3-11%. Discussion. Estimates of elastic modulus agree closely with those previously reported from direct measurements obtained via mechanical tensile tests on major weight bearing tendons in vitro [1,2]. Hysteresis derived from models of the stress-strain relationship is consistent with direct measures from various mamalian tendon (7-10%) but is lower than previous estimates in human tendon (17-26%) [3]. This non-invasive method would appear suitable for monitoring changes in tendon properties during dynamic sporting activities.