Medicine & Science in Sports & Exercise:
The Acute Transverse Strain Response of the Patellar Tendon to Quadriceps Exercise
WEARING, SCOTT C.1,2; HOOPER, SUE L.2; PURDAM, CRAIG3; COOK, JILL4; GRIGG, NICOLE5; LOCKE, SIMON2; SMEATHERS, JAMES E.5
1Faculty of Health Sciences and Medicine, Bond University, Queensland, AUSTRALIA; 2Centre of Excellence for Applied Sport Science Research, Queensland Academy of Sport, Queensland, AUSTRALIA; 3Department of Physical Therapies, Australian Institute of Sport, ACT, AUSTRALIA; 4Faculty of Medicine, Nursing and Health Sciences, Monash University, Victoria, AUSTRALIA; and 5Institute of Health and Biomedical Innovation, Queensland University of Technology, Queensland, AUSTRALIA
Address for correspondence: Scott C. Wearing, Ph.D., Faculty of Health Sciences and Medicine, Bond University, Gold Coast, Qld 4229, Australia; E-mail: firstname.lastname@example.org.
Submitted for publication June 2012.
Accepted for publication October 2012.
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 yr; height, 1.75 ± 0.09 m; and weight, 76.7 ± 12.3 kg) free of knee pain participated in the research. A 10- to 5-MHz linear array transducer was used to acquire standardized sagittal sonograms of the right patellar tendon immediately before and after 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 preexercise tendon thickness and expressed as a percentage. Measures of tendon echotexture (echogenicity and entropy) were also calculated from subsequent grayscale profiles.
Results: Quadriceps exercise resulted in an immediate decrease in patellar tendon thickness (P < 0.05), equating to a transverse strain of −22.5% ± 3.4% and was accompanied by increased tendon echogenicity (P < 0.05) and decreased entropy (P < 0.05). The transverse strain response of the patellar tendon was significantly correlated with both tendon echogenicity (r = −0.58, P < 0.05) and entropy after exercise (r = 0.73, P < 0.05), whereas older age was associated with greater entropy of the patellar tendon before exercise (r = 0.79, P < 0.05) and a reduced transverse strain response (r = 0.61, P < 0.05) after exercise.
Conclusions: This study is the first to show that quadriceps exercise invokes structural alignment and fluid movement within the matrix that are manifested by changes in echotexture and transverse strain in the patellar tendon.
Little is known about the adaptive response of the human patellar tendon to physical activity. Most, but not all (24), studies have observed that habitually active individuals possess larger tendons (20%–36%) than untrained individuals (33,39), with the most pronounced differences coinciding with sites of peak strain at the proximal or distal aspects of the tendon (12,31). Similarly, recent prospective studies in healthy young adults have demonstrated that short-term resistance training (9–14 wk) increases tendon stiffness in vivo and induces region-specific tendon hypertrophy (2,42), which in the case of the patellar tendon was comparable with that of the quadriceps muscle (approximately 6%) itself (28,41). This finding, however, is not universal. Similar training protocols have been shown to have negligible influence on patellar tendon size (27), especially in older adults (60–80 yr) (38,42).
In contrast to the effects of resistance training and habitual loading, acute bouts of exercise appear to induce the exact opposite effect in tendon over the short term (<24 h). Marked, although transient, decreases in tendon thickness have been commonly reported in the Achilles tendon on completion of resistive ankle exercise (20,26,45,46) and after walking and running (14). Equating to transverse strains of about 15% (20,26,45,46), these conditioning effects have been widely reported by studies investigating the mechanical properties of tendon in vitro and have been suggested to reflect convective movement and extrusion of fluid from the tendon midsubstance (30,32). Although load-induced fluid movement and subsequent shear stress have been hypothesized to play an important role in tendon homeostasis and the transport of high molecular weight solutes such as growth factors and cytokines (23), in vivo observations of the acute transverse strain response of tendon to date have been limited to the Achilles tendon.
Although all tendons act as force conduits, transmitting force generated by its associated muscle, internal stress distributions will differ depending on whether they contain a myotendinous junction or a sesamoid bone. Nonuniform activation of muscle fibers/compartments across a myotendinous junction would, in theory, result in uneven internal stresses and tendon deformation (4,5), thereby altering intratendinous shear loads and fluid movement (1). Eccentric contractions will further exaggerate this effect (22). However, the patellar tendon with its unique anatomy of bony attachments at the deeper part of each end is likely to be subjected to more uniform loads compared with tendons, such as the Achilles, that do not contain sesamoid bones (6). There is a need, therefore, to establish whether the acute transverse strain response that occurs with exercise in the Achilles tendon also occurs in the patellar tendon.
The aim of the current study, therefore, was to evaluate the immediate response of the patellar tendon to a bout of quadriceps exercise. Specifically, we tested the null hypothesis that the resistive exercise would not significantly alter sonographic measures of patellar tendon structure or transverse strain.
A convenience sample of 12 healthy adult males was re-cruited from a university faculty to participate in the study (Table 1). Their mean age (±SD) was 34.0 ± 12.1 yr (range, 23–57 yr), with a mean height of 1.75 ± 0.09 m and bodyweight of 76.7 ± 12.3 kg. Participants were nonsmokers, not taking any medication, and recreationally active based on self-report. No participant reported a medical history of diabetes, inflammatory joint disease, familial hypercholesterolemia, or patellar tendon pain or pathology. Participants gave their written informed consent to the procedures of the study, which received approval from the institutional Ethical Committee review board.
All participants reported to the laboratory having abstained from vigorous physical activity and consumption of alcohol in the previous 24 h. Body height was measured to the nearest millimeter using a Harpenden stadiometer (Cranlea and Co, Birmingham, UK), and body weight was recorded to the nearest gram with clinical scales (Tanita, Tokyo, Japan). Body mass index (BMI) was calculated by dividing body weight (kg) by the square of body height (m).
Sonographic examination of the patellar tendon was undertaken by a single operator using a 10- to 5-MHz linear array transducer (Echoblaster 128; UAB Telemed, Vilnius, Lithuania) with standardized settings and acquisition protocol. The spatial pulse length and axial resolution of the system was 310 and 160 μm, respectively. In accordance with previous recommendations, longitudinal sonograms of the tendon were acquired perpendicular to the point of maximum tendon width (15). Particular care was taken to position the transducer perpendicular to the tendon surface. All sonograms were acquired with participants supine and with their knee at 90° (15).
After preexercise sonograms, participants completed 90 repetitions of double-leg parallel-squat exercises in which they moved from standing erect to a position of 90° of knee flexion and then back in time with an oscillogram display. Each squat was performed at a rate of approximately 0.25 Hz and involved a 2-s period of ascent and 2-s period of descent (16). Exercises were performed in a Smith machine with an Olympic bar weighted so as to achieve an effective resistance of 175% bodyweight (additional 75% bodyweight added). The loading parameters were similar to rehabilitation protocols commonly used in the management of patellar tendinopathy and induced tensile loads in the patellar tendon comparable with that experienced during running (16,37,40). Longitudinal sonograms were repeated immediately after completion of the quadriceps exercises. In total, the exercise protocol took around 6 min to complete.
Data reduction and statistical analysis.
Sonographic images were exported in DICOM format and analyzed using MATLAB software (MathWorks Inc., Natick, MA). The anterior and posterior edges of the tendon were identified with the aid of a grayscale profile, and tendon thickness was determined at a standard site, 20 mm distal to the attachment at the inferior pole of the patella (Fig. 1) (15). Transverse Hencky strain (%) was calculated as the natural log of the ratio of post- to preexercise tendon thickness and expressed as a percentage (43). The coefficient of variation for repeated measures was 2.6%.
On sonography, normal tendons are characterized by a regular heterogeneous echo pattern of alternating light and dark striations with a wide range of grayscale values. Measures of sonographic echotexture, therefore, primarily reflect the density and arrangement of the collagenous matrix and are often more homogenous and reduced (hypoechoic) in degenerative pathologies, such as tendinopathy (10). Although quantification of sonographic echotexture has been shown to be sensitive in detecting neuromuscular disorders (25,36), the technique has been less commonly used to evaluate tendon. In the current study, tendon echotexture was characterized by two first-order statistical parameters (echogenicity and entropy) determined over a rectilinear region of interest bound by the anterior and posterior borders of the tendon and an equivalent number of pixels proximal and distal to the measurement site. Tendon echogenicity was estimated by calculating the mean grayscale value (arbitrary units (U) within the region of interest (10). Grayscale values ranged between 0 and 255, with higher values indicative of a hyperechoic tendon. Tendon entropy (H), a statistical measure of tendon homogeneity or the randomness of collagen orientation with arbitrary units (U), was estimated within the region of interest by calculating the average value of the log of the probability density function of the grayscale histogram (17), and it is given by the following equation:
Equation (Uncited)Image Tools
where px denotes the probability, a grayscale value x is occupied within the region of interest, and R denotes the upper grayscale limit. As such, entropy is related to the local variance of the intensity histogram of the region of interest (48). Low entropy values depict tendon homogeneity, whereas high values reflect collagen disorder (17). The coefficient of variation for repeated measures of tendon echogenicity and entropy was 5.5% and 2.0%, respectively.
The Statistical Package for the Social Sciences (SPSS Inc, Chicago, IL) was used for all statistical procedures. Kolmogorov–Smirnov tests were used to evaluate data for underlying assumptions of normality. Outcome variables were determined to be normally distributed, so means and SD were used as summary statistics. Paired t-tests were used to evaluate potential changes in tendon thickness and echogenicity immediately postexercise. Relationships between transverse tendon strain and anthropometric variables were investigated using scatter plots and Pearson product–moment correlations. An alpha level of 0.05 was used for all univariate tests of significance.
The sagittal thickness of the patellar tendon significantly decreased immediately after quadriceps exercise (t = 14.9, P < 0.05), resulting in a mean transverse strain of −22.5% ± 3.4% (Table 2).
There were no significant correlations noted between the magnitude of the transverse strain response of the patellar tendon and measures of height, weight, or BMI. However, there was a significant negative correlation between transverse patellar tendon strain and participant age (r = 0.61, P < 0.05; Fig. 2).
The average grayscale of the patellar tendon was significantly higher (t = −3.6, P < 0.05) and average entropy significantly lower (t = 2.7, P < 0.05) immediately after exercise (Table 1). Although there were no statistically significant correlations noted between tendon echogenicity and anthropometric variables (height, weight, and BMI), age was positively correlated with the entropy of the tendon before exercise (r = 0.79, P < 0.05). Similarly, the transverse strain response of the patellar tendon was significantly correlated with both tendon echogenicity (r = −0.58, P < 0.05) and entropy (r = 0.73, P < 0.05) after exercise. Larger transverse strains were associated with greater echogenicity (Fig. 3) and lower entropy of the tendon postexercise.
To our knowledge, this is the first study to examine the immediate transverse strain response of the patellar tendon to quadriceps exercise. We observed an immediate decrease in patellar tendon thickness, equating to a transverse strain of −22%, in response to exercise. This is similar to the reductions in tendon size (15%–20%) observed in the Achilles tendon immediately after intense or prolonged ankle exercise (14,19,20,26,45,46). Transverse tendon strains have previously been hypothesized to reflect fluctuations in the fluid content of the tendon matrix associated with load-induced alignment of collagen and reduction of crimp (46) and are consistent with in vitro observations of the extrusion and visible loss of water from tendon exposed to load (23,30,47). Our observations that larger transverse strains were associated with greater echogenicity and lower entropy of the patellar tendon postexercise lend further support to this mechanism.
The magnitude of the transverse strain response of the patellar tendon to exercise in the current study was independent of measures of body anthropometry but was negatively correlated with participant age. This is a novel finding, and Figure 2 shows that with each decade of life, there was a 2% reduction in the transverse strain response of the patellar tendon after exercise, suggesting that exercise invoked less collagen alignment and intratendinous fluid movement in older individuals. Interestingly, age was also correlated with greater entropy of the patellar tendon before exercise (R2 = 0.63) in this study, suggesting that aging tendon was, in part, associated with a more disorganized collagen structure. These findings are consistent with changes in the composition of the patellar tendon noted with senescence, which include altered fibril morphology, an increase in collagen cross-linking, a decrease in glycosaminoglycan concentration, and lowered water content (11,44). Given that interstitial fluid movement is thought to play a key role in mechanotransduction and tendon homeostasis (23), it may be speculated that diminished solid phase alignment and fluid movement with aging, as evidenced by a lower transverse strain response to exercise, may contribute to the impaired adaptive capacity of the patellar tendon in older individuals noted in previous research (42). In support of such a concept, changes in tendon entropy and a lower transverse strain response of the Achilles tendon to exercise have been previously reported with clinical tendinopathy (10,21). Measurement of acute transverse tendon strain and its recovery in response to a defined exercise (loading impulse) may, therefore, potentially provide clinicians and sports scientists with an index for evaluating tendon resilience in athletes. It is noteworthy, however, that none of the participants in this study reported a history of tendon pain, suggesting that age-specific estimates of tendon response may be necessary if adequate benchmarking is to be undertaken. Given the relatively small sample size of the current study, further research that monitors the acute response of the patellar tendon in a wide range of age groups both with and without tendinopathy is required before more definitive conclusions can be made.
Although the spatial resolution of ultrasonography makes it ideal for imaging the patellar tendon and allows for precise localization of the tendon boundary, it is recognized that the technique is also highly user dependent. The coefficient of variation for repeated measures of patellar tendon thickness in the current study (2.6%), however, was relatively small compared with the overall effect of quadriceps exercise (−22% strain). Moreover, the mean preexercise thickness of the patellar tendon in the current study (3.0 mm) is consistent with the lower range of values reported within the literature (15,18). It is noteworthy that this study did not include the paratenon within measures of patellar tendon thickness. This loose connective tissue layer, which is about 0.4 mm thick at rest (15), undergoes marked expansion with exercise in association with dilation of blood vessels (7). Such exercise-induced changes in the paratenon, therefore, would oppose those of the tendon proper and artificially mask the decrease in tendon thickness noted immediately postexercise in this study. Consequently, we advocate that measures of patellar tendon thickness are made from longitudinal sonograms, which, in contrast to transverse plane images, allow easy visualization of the paratenon and have been shown to yield more accurate and reliable tendon thickness measurements (15).
A limitation of this study is that it determined the sagittal thickness and one-dimensional strain response of the patellar tendon at a single site, 20 mm distal to the inferior pole of the patella. Thus, it is unknown if the effects of exercise result in similar mediolateral strains in the patellar tendon or whether exercise-induced strains are uniform across the entire tendon structure. Although there is evidence that mechanical properties of tendon are transversely isotropic (29) and similar reductions in mediolateral tendon thickness, albeit in the Achilles, have been observed with loading (26), there is also evidence that tendon composition may vary along its length and that axial and transverse properties of the patellar tendon may be regionally heterogeneous (9,13,26). Consequently, further research evaluating transverse strains in two dimensions (anteroposterior and mediolateral), at multiple sites along the length of the tendon, and in pathological patellar tendons with varied compositional states is warranted.
Emerging evidence suggests that the mechanical response of tendon to exercise may be sensitive to both the magnitude and rate of strain as well as the mode of muscle contraction (3,20). The clinical exercise protocol used in the current study (concentric and eccentric muscle contraction) was sufficient to induce alterations in patellar tendon structure. However, the relative contribution of contraction type and of individual components of the loading stimulus (magnitude, frequency, and duration), which influence the rate and duration of loading, on the magnitude of the acute transverse strain response of the patellar tendon remains unknown. Similarly, the mechanical response and properties of tendon may differ between males and females (35). Although sex differences in patellar tendon properties are not universally reported (34) and may even be moderated by age (8), it is important to note that this study was limited to evaluating the transverse strain response of the patellar tendon in a small sample of healthy adult males without a history of tendinopathy. The transverse strain response observed in the current study, therefore, may not be directly transferable to female cohorts in those of younger or older age or in individuals with a history of tendinopathy. Nonetheless, the findings of the current study suggest that quadriceps exercise results in a more organized collagen structure and movement of interstitial fluid within the patellar tendon of adult males, which are manifested by changes in tendon echotexture and transverse strain. Given that load-induced fluid movement likely plays an important role in mechanotransduction and tendon homeostasis (23), future research directed toward identifying both intrinsic (participant specific) and extrinsic (external loading) factors that influence the transverse strain response of the patellar tendon and its recovery is needed.
This study is the first to show that acute mechanical loading of the patellar tendon via quadriceps exercise results in an immediate decrease in patellar tendon thickness in vivo, which is accompanied by changes in tendon echotexture. This response to exercise, which is diminished with advancing age, affords new insights into the acute response of the patellar tendon to load.
The authors would like to thank Timothy Gurnett (High Performance Computing, Queensland University of Technology, Queensland, Australia) for his assistance with data processing.
This research was funded by an Australian Research Council linkage grant. Dr. Wearing is funded through a Smart Futures Fellowship, Department of Employment, Economic Development and Innovation, Queensland Government.
The authors declare no conflicts of interest, financial or otherwise.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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BIOMECHANICS; TENDON; ULTRASOUND; COLLAGEN
©2013The American College of Sports Medicine
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