Alterations in Mechanical Properties of the Patellar Tendon Is Associated with Pain in Athletes with Patellar Tendinopathy
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Eur J Appl Physiol DOI 10.1007/s00421-017-3593-1 ORIGINAL ARTICLE Alterations in mechanical properties of the patellar tendon is associated with pain in athletes with patellar tendinopathy W. C. Lee1 · Z. J. Zhang2 · L. Masci3 · G. Y. F. Ng1 · Siu Ngor Fu1 Received: 4 December 2016 / Accepted: 19 March 2017 © Springer-Verlag Berlin Heidelberg 2017 Abstract found between tendon stiffness and pain during a single- Purpose To compare tendon strain and stiffness between legged declined-squat test (r = 0.30, P = 0.09). athletes with patellar tendinopathy and healthy controls, Conclusion Our findings show that tendon strain is and explore whether the intensity of pain and dysfunction reduced in athletes with patellar tendinopathy, and a lower were related to the mechanical properties of the tendon. tendon strain is associated with a greater magnitude of pain Methods Thirty-four male athletes with patellar tendi- perceived. nopathy and 13 healthy controls matched by age and activ- ity levels were recruited. The in vivo mechanical properties Keywords Patellar tendinopathy · Tendon strain · Tendon of the patellar tendon were examined by ultrasonography pain · Tendon function and dynamometry. In subjects with patellar tendinopathy, the intensities of self-perceived pain (maximal pain in the Abbreviations past 7 days and pain during a single-legged declined-squat BF Biceps femoris test) using the visual analogue scale and the assessment of BMI Body mass index functional disability using the Victorian Institute of Sport d Deformation Assessment—patellar questionnaire, were collected. F Force Results In subjects with patellar tendinopathy, tendon L Length strain was significantly reduced by 22% (8.9 ± 3.7 vs. MDD Minimal detectable differences 14.3 ± 4.7%, P = 0.005) when compared with healthy con- PMA Patellar tendon moment arm trols. There was no significant group difference in ten- RMS Root mean square don stiffness (P = 0.27). Significant negative correlations SD Standard deviation between tendon strain and the maximal self-perceived US Ultrasound pain over 7 days (r = −0.37, P = 0.03), and pain during a VAS Visual analogue scale single-legged declined-squat test (r = −0.37, P = 0.03) were VISA-p Victorian Institute of Sport Assessment detected. A trend of significant positive correlation was Communicated by Olivier Seynnes. Introduction * Siu Ngor Fu Tendon overload is believed to be one of the major etio- [email protected] logical factors for tendinopathy, which results in pain and 1 Department of Rehabilitation Sciences, The Hong dysfunctions (Magnusson et al. 2010). Histopathologi- Kong Polytechnic University, Hung Hom, Kowloon, cal examinations reveal discontinuous and disorganized Hong Kong SAR, China collagen fibers (Aström and Rausing 1995; Kalebo et al. 2 Department of Physical Therapy, Luoyang Orthopedic 1991) and substantial increase of mucoid ground substance Hospital of Henan Province, Luoyang, Henan, China (Khan et al. 1996) in a pathologic tendon. These changes 3 Pure Sports Medicine, London, UK Vol.:(0123456789)1 3 Eur J Appl Physiol in tendon morphology might induce mechanical changes in also reported after the exercise programme. Such findings the pathological tendons. suggest a possible relationship between tendons’ mechani- Possible changes in the mechanical properties of path- cal properties and the magnitude of tendon-related pain in ologic patellar tendon have been studied but with incon- subjects with tendinopathy. sistent findings (Couppé et al. 2013; Helland et al. 2013; This study aimed to compare tendon mechanical prop- Kongsgaard et al. 2009, 2010). Kongsgaard et al. (2009) erties between athletes with pathologic tendon and healthy were the first group to use ultrasonography and dynamom- control. Possible relationships between tendon mechani- etry to compare tendons’ mechanical properties between cal properties and the intensity of tendon-related pain and the painful and non-painful sides in subjects with unilat- dysfunction would be explored. We hypothesized that (1) eral patellar tendinopathy. The authors observed reduced tendon stiffness and strain would be altered in athletes with tendon stiffness in the painful leg. The difference, however, patellar tendinopathy compared with healthy controls and could not reach a statistically significant value. Heales et al. (2) tendon stiffness and tendon strain would be associated (2014) suggested that deficits in motor systems are present with the intensity of tendon-related pain and dysfunction. bilaterally in unilateral tendinopathy. The contralateral Findings from this study would shed the light on the influ- and non-painful could not be regarded as “healthy” con- ence of tendon mechanical properties, impairments, and trol. When tendon mechanical properties were compared dysfunctions in patellar tendinopathy. between subjects with tendinopathic tendon and healthy individuals, Kongsgaard et al. (2010) detected a no signifi- cant reduction in tendon stiffness and increased strain on 8 tendinopathic tendon compared with 9 controls. Similarly, Methods Couppé et al. (2013) observed no significant group dif- Ethics statement ferences on tendon stiffness and strain on elite badminton players with pathological tendon and controls. On the con- This study was approved by the Human Subject Ethics trary, Helland et al. (2013) recruited young volleyball play- Sub-committee of the administrating institution. The exper- ers and reported significantly lower tendon stiffness and imental procedures were conducted in accordance with the modulus on the pathological group compared with healthy Declaration of Helsinki. The procedures of the study were controls. In Helland’s study, young athletes involving in fully explained to the participants and they provided their jumping sports were recruited. However, the dysfunction informed written consent before testing. scores in the pathological group were relatively high. It is unclear whether such changes on tendon mechanical prop- erties would be modulated in athletes with patellar tendi- Subject recruitment nopathy with lower functional scores, i.e., Victorian Insti- tute of Sport Assessment (VISA-p) less than 80 (Visentini Thirty-four male subjects with patellar tendinopathy were et al. 1998; Zwerver et al. 2011). recruited from local volleyball, basketball, and handball Ultrasound imaging with dynamometry was used to teams. Subjects were included if they had a history of pain capture tendon images and force during ramped maximum during activity/training at the inferior pole of the patellar voluntary isometric contraction. Elastic modulus was com- with visual analogue scale (VAS) equal to or greater than puted based on a number of assumptions. One of them is 2 for at least 3 months and with a VISA-p questionnaire tendon unity. However, pathological change including score less than 80 (Visentini et al. 1998; Zwerver et al. hypoechoic area or a fibrotic knot has been reported in the 2011). Clinical tests such as palpation of the inferior pole proximal and dorsal region of a tendon (Aström and Raus- of patella elicited comparable pain. Thickening of the prox- ing 1995; Kalebo et al. 1991) which signifies that the ten- imal part of the patellar tendon with an area of hypoechoic don might not have a uniform dimension. A recent review signals was detected under ultrasonographic examination commented that the calculation process with in vivo tendon (Kulig et al. 2013). A physical therapist with 15 years of testing might introduce a certain amount of error (Seynnes experience in treating musculoskeletal-related injuries con- et al. 2015). The authors suggested that primary measure- ducted the clinical tests. Subjects were excluded if they ments, such as tendon stiffness and strain could be used to suffered from patellofemoral pain syndrome, fat pad irrita- reflect tendon mechanical properties. tions, meniscal injury, osteoarthritis, rheumatoid arthritis, Are tendon mechanical properties associated with pain or infection; had a history of fracture of the lower limbs or dysfunction in subjects with patellar tendinopathy? and inflammatory myopathies; and had received cortisone Kongsgaard et al. (2010) reported significant reduction of injections and other interventions within 3 months. tendon stiffness after a heavy slow resistance training pro- Thirteen healthy subjects without any knee problems gramme. Clinical improvement on pain and function was matched by age and activity level were recruited. 1 3 Eur J Appl Physiol In vivo tendon mechanical property examination using standardized warm-up with 5 min of low intensity exercise ultrasonography and dynamometry on a stationary bike and two sets of five repetitions of 10-s static stretching of quadriceps and hamstrings before test- The procedure was adopted from the studies of Kubo et al. ing. The subject also performed 4–7 smooth ramped knee (2006) and Reeves et al. (2003). An isokinetic dynamom- isometric extensions with visual feedback using a torque eter (HUMAC® NORM, Cybex, International Inc., USA) gauge with 90 s of rest in between. In the second session, was used to capture the torque output during maximum a similar procedure was conducted—four contractions with isometric knee extension at 90° of knee flexion (full exten- ramped knee extensions with the maximal effort to obtain sion = 0°). Subjects sat with the knee joint axis aligned clear ultrasound images. Each contraction lasted for 10 s. against the dynamometer axis of rotation (Fig. 1). Torque signals were converted at a sampling