Tendinopathy Alters Cumulative Transverse Strain in the Patellar Tendon after Exercise : Medicine & Science in Sports & Exercise

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Tendinopathy Alters Cumulative Transverse Strain in the Patellar Tendon after Exercise

WEARING, SCOTT C.1, 2; LOCKE, SIMON2; SMEATHERS, JAMES E.1; HOOPER, SUE L.2

Author Information
Medicine & Science in Sports & Exercise: February 2015 - Volume 47 - Issue 2 - p 264-271
doi: 10.1249/MSS.0000000000000417
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Abstract

Patellar tendinopathy (jumper’s knee) is a common musculoskeletal condition in elite athletes, with prevalence ranging from 14% in runners to 45% in elite jumping athletes (28). Although the etiology is poorly understood, tendinopathy is generally considered to be an “overuse” condition in which the tendon fails to adapt its material and structural properties to prevailing loading conditions. In comparison with healthy tendons, lower axial stiffness, elastic modulus, and greater creep have been commonly observed in Achilles tendinopathy (2). However, such differences have not been routinely reported in patellar tendinopathy (8,17,23). Currently, relatively little is known about the acute adaptive response of the patellar tendon to exercise or its interaction with tendon pathology.

Although most studies have observed that habitually active adults possess a larger patellar tendon cross-sectional area (20%–30%) than untrained adults (7), longitudinal studies have shown that exercise training for 3 months (180–200 repetitions of 80% of one-repetition maximum completed 3–4 times per week) either increases (32) or has no effect on measures of patellar tendon stiffness and elastic modulus in healthy individuals (25). Whereas these discrepancies may partly reflect differences in contraction type and loading impulse in the patellar tendon, acute bouts of intense cyclic exercise, in contrast, have been commonly observed to produce transient decreases in tendon thickness (13,15,43–45). Equating to transverse strains of around 15%, these creep-related effects have been widely reported by studies investigating the mechanical properties of tendon in vitro and have been conjectured to reflect movement of interstitial fluid associated with load-induced alignment of the solid phase of tendon matrix (16,27). Load-induced fluid movement and subsequent shear stress each play an important role in mechanotransduction and tendon homeostasis (42), and reduced fluid movement has been implicated in the progression of Achilles tendinopathy (15). However, to date, the effect of tendinopathy on the transverse strain response of the patellar tendon has not been investigated.

The purpose of this research, therefore, was to evaluate the effect of tendinopathy on sonographic characteristics, Doppler flow, and acute transverse strain response of the patellar tendon to exercise. We tested the null hypothesis that patellar tendinopathy would have no significant effects on tendon structure, Doppler flow, and transverse tendon strain immediately after exercise.

METHODS

Nine young adults with unilateral patellar tendinopathy and 10 healthy control adults who competed in Australian state or reserve league volleyball competitions participated in the study. All participants were members of the Queens land Elite Development Volleyball Program, were nonsmokers, nonmedicated, and participated in the same volleyball-specific training program, which incorporated a minimum of 14 h·wk-1 of physical activity (skills development training, strength and conditioning and match play), on the basis of self-report. No participant reported medical history of diabetes, inflammatory joint disease, or familial hypercholesterolemia. All participants with patellar tendinopathy presented with pain and sensation of stiffness particularly at the onset of loading activities, focal thickening of the involved tendon, and unilateral symptoms for greater than 6 wk. Participants with tendinopathy reported a mean Victorian Institute of Sport Assessment for patellar tendinopathy (VISA-P) score of 70 ± 11, where a score of 0 represents worst symptoms possible and a score of 100 represents no symptoms. All participants provided a written informed consent to the procedures of the study, which received approval from the institutional ethical committee review board. Participant numbers were sufficient to detect a 5% difference in the immediate transverse strain response of the two tendons ([alpha] = 0.05, [beta] = 0.20) on the basis of previously published data for human tendon (44).

All participants reported to the laboratory, having abstained from vigorous physical activity and consumption of alcohol in the previous 12 h. Body height was measured to the nearest millimeter using a Harpenden stadiometer (Cranlea and Co., Birmingham, United Kingdom), 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 7.2- to 14-MHz multifrequency linear array transducer (plt–1204ax and Aplio XG SSA–770A/80; Toshiba, Tokyo, Japan) with standardized settings and acquisition protocol (44). Longitudinal sonograms of the tendon were acquired perpendicular to the point of maximum tendon width, and particular care was taken to position the transducer perpendicular to the tendon surface and parallel to the fiber direction, as previously described (34). All sonograms were acquired with participants supine and with the knee flexed at 90° to the leg (44). The accuracy and precision of the ultrasound system were evaluated by undertaking repeated measurements of a standard calibration phantom (040GSE; CIRS, Norfolk, VA) consisting of a number of Nylon monofilaments of varying diameters (0.1–8.0 mm) and depths embedded within a tissue-mimicking material (attenuation, 0.5 ± 0.05 dB·cm-1·MHz-1). The 95% limit of agreement for repeated measures of 27 separate calibration monofilaments was ±100 μm.

Each tendon was also examined for intratendinous microvessels using broadband power Doppler with an “advanced dynamic flow” frequency of 10 MHz, pulse repetition frequency of 6.1 kHz, color velocity of 3.1 cm·s-1, a region of interest (ROI) of 2.5 × 1.1 cm, and color intensity set marginally below the artefact threshold. For these measurements, participants were positioned supine with their knee fully extended and pressure applied to the probe was kept to a minimum to avoid obliteration of small vessels (9).

After preexercise sonograms, participants completed 45 repetitions of a double-leg parallel squat exercise in which they moved from standing erect to a position of 90° of knee flexion and back. 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. Exercises were performed in a Smith machine with an Olympic bar weighted, so as to achieve an effective resistance of 145% body weight. All exercises were performed on a standard 25° decline board. Longitudinal grayscale and Doppler sonograms were repeated within 1 min of 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 superficial and deep edges of the tendon were identified with the aid of a grayscale profile, and tendon thickness was determined at two standard sites, 5 and 25 mm distal to the attachment at the inferior pole of the patella (Fig. 1a). Transverse Hencky strain (%) was calculated as the natural log of the ratio of post- to preexercise tendon thickness and expressed as a percentage. The within-subject coefficient of variation for repeated measurements of transverse strain in the patellar tendon was 2.1%.

F1-7
FIGURE 1.:
Patellar tendon thickness was measured 5 (L1) and 25 mm (L2) inferior to the patella pole with the aid of a grayscale profile. At each site, average grayscale in the superficial (S1 and S2) and deep (D1 and D2) aspects of the tendon were determined (A). Illustration of the intratendinous PDU within a 2.5 × 1.1 cm ROI graded using the modified Öhberg score (B). The area of the same intratendinous PDU flow was also quantified by determining the number of color pixels within the tendon and the square of effective pixel resolution. The bias and limits of agreement for repeated measurements of area was -0.01 ± 0.6 mm2 (C).

Tendon echogenicity in the superficial and deep aspects of the patellar tendon was estimated by calculating the mean grayscale value (arbitrary units (U)) within two rectilinear ROI. At each site, a rectilinear ROI was initially created in which the length of all four sides equated to 90% of the measured tendon thickness. The ROI was positioned equally between and centered about the digitized superficial and deep tendon borders. The ROI at each site was subsequently bisected to form an equally sized deep and superficial ROI. Thus, the superficial ROI was bound by the anterior border and midsection of the tendon and an equivalent number of pixels proximal and distal to the measurement site (Fig. 1a). Likewise, the deep ROI was bound by the midsection and posterior border of the tendon and an equivalent number of pixels proximal and distal to the measurement site (44). It was hypothesized that analysis of the patellar tendons from a regional point of view may support recent work suggesting that there is a difference in the strains experienced between the posterior fibers of the tendon and those of the anterior region (10). Grayscale values within the ROI ranged between 0 and 255, with higher values indicative of a hyperechoic tendon. The coefficient of variation for repeated measures of tendon echogenicity was 5.5%.

Intratendinous power Doppler flow (PDU) was qualitatively graded from 0 to IV using the modified Öhberg score (9,34). In brief, tendons were scored 0 when no vessels were visible and I–IV when one to four or more vessels were visible within the 2.5 × 1.1 cm ROI. PDU images were independently scored by two examiners blinded to the case history of the participants and with 100% agreement. PDU signal was also quantitatively assessed using a modified version of a previously described method (31), in which PDU area was calculated as the product of the number of color pixels within the tendon and the square of effective pixel resolution (Fig. 1b and c). The limits of agreement for repeated measurements of PDU area was ±0.6 mm2.

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. Between-group differences in body anthropometry were investigated using independent t-tests. The effect of exercise on tendon thickness was evaluated using a repeated-measures ANOVA model within a generalized linear modeling framework, in which site (proximal/distal) and exercise (pre/post) were treated as within-subjects factors whereas limb (control left/control right/asymptomatic/symptomatic) was treated as a between-subject factor. Between-group differences in average tendon grayscale were evaluated within a generalized linear modeling framework using three-way repeated-measures ANOVA in which region (superficial/deep), site (proximal/distal), and exercise (pre/post) were treated as within-subject factors. Where appropriate, significant interactions between factors were investigated further with separate one-way ANOVA in combination with the Tukey post hoc analysis. Differences in qualitative grade of neovascularization after exercise were evaluated using a Wilcoxon signed rank test, whereas differences in PDU area were assessed using a paired t-test. Potential relations between PDU area and symptom severity (VISA-P scores) were evaluated using Pearson product moment correlations. An alpha level of 0.05 was used for all univariate tests of significance.

RESULTS

The anthropometric characteristics of participants are summarized in Table 1. There was no statistically significant difference in the mean age, weight, or BMI of participants with and without patellar tendinopathy. However, participants with patellar tendinopathy were 5% taller than healthy controls (t = -3.58, P = 0.002).

T1-7
TABLE 1:
Demographic characteristics of participants.

On sonography, normal healthy tendons were characterized by a regular structure and heterogeneous echo pattern of alternating light and dark striations with a wide range of grayscale values. In contrast, patellar tendinopathy was characterized by changes in both tendon ultrastructure and echotexture. There was significant interaction between site and limb for measures of tendon thickness (F = 7.5, P = 0.001). Post hoc analysis revealed a significantly thicker tendon in the symptomatic limb compared with asymptomatic and healthy tendons at both the proximal (F = 7.3, P < 0.05) and distal (F = 4.9, P < 0.05) measurement sites (Fig. 2). Repeated-measures ANOVA also identified significant interaction between tendon region and limb for measures of average grayscale (F = 2.8, P = 0.05). Post hoc analysis demonstrated that tendon echogenicity was significantly lower in the deep, rather than in the superficial, region of symptomatic and asymptomatic patellar tendons when compared with healthy controls at the proximal (F = 4.4, P < 0.05) measurement site (Fig. 3). Six of the nine participants with patellar tendinopathy (67%) also presented with signs of neovascularity with PDU. When present, neovascularization grades ranged between I and IV before exercise, with a median of IV. PDU area at baseline was moderately correlated with VISA-P score (r = -0.58, P = 0.05), such that greater PDU area before exercise was associated with lower (worse) symptom severity scores. Microvascularity was not present in the tendons of healthy participants.

F2-7
FIGURE 2.:
Patellar tendon thickness in symptomatic, asymptomatic and left and right control limbs measured 5 (site 1) and 25 mm (site 2) inferior to the patella pole. *Significantly different from all other limbs at the given site (P < 0.05). †Statistically significant main effect for site (P < 0.05).
F3-7
FIGURE 3.:
Mean grayscale in the superficial and deep aspects of the patellar tendon before (pre) and after (post) exercise in symptomatic, asymptomatic, and left and right control limbs and determined at two sites, as follows: 5 mm distal to the inferior pole of the patella (A) and 25 mm distal to the inferior pole of the patella (B). Note that although average grayscale was significantly lower in both symptomatic and asymptomatic tendon, there was a statistically significant main effect for exercise in all tendons (P < 0.05).

Exercise resulted in immediate decrease in patellar tendon thickness in healthy tendons at both proximal and distal measurement sites, which equated to a cumulative transverse strain of approximately 6% (Fig. 4). There was a significant main effect for limb in the cumulative transverse strain response of the patellar tendon to exercise (F = 8.5, P < 0.001). Post hoc analysis revealed that cumulative transverse strain was significantly lower in symptomatic tendons than that in asymptomatic and healthy tendons (P < 0.05).

F4-7
FIGURE 4.:
Cumulative transverse strain in the patellar tendon in symptomatic, asymptomatic, and control limbs after exercise. Strain was determined 5 (site 1) and 25 mm (site 2) distal to the inferior pole of the patella. *Significantly different from all other limbs at the given site (P < 0.05).

As shown in Figure 3, there was a significant main effect of exercise on tendon grayscale (F = 28.8, P < 0.001), with increase in tendon echogenicity occurring after exercise. In addition, exercise resulted in significant reduction in PDU area in those with PDU signal, decreasing by 57%, from 9.3 ± 8.3 mm2 before exercise to 5.3 ± 7.2 mm2 immediately after exercise (t = 2.0, P = 0.05). As shown in Figure 5, postexercise change in PDU area was positively correlated (r = 0.93, P = 0.008) with VISA-P score, such that greater postexercise reductions in PDU were associated with lower (worse) symptom severity scores. There was, however, no statistically significant effect of exercise on the qualitative microvascularity score in symptomatic tendon (median score after exercise, II; range, 0–IV; Z = -1.633; P = 0.102).

F5-7
FIGURE 5.:
The relation between symptom severity (VISA-P) and change in PDU area in the infrapatellar tendon immediately after exercise.

DISCUSSION

To the best of our knowledge, this is the first study to show that the cumulative transverse strain response of the patellar tendon to exercise is impaired in the presence of tendinopathy. The transverse strain response of tendon to loading has been previously hypothesized to reflect interstitial fluid movement associated with the load-induced alignment of collagen and reduction of crimp (45) and is consistent with in vitro observations of axial creep and extrusion of water from tendons exposed to tensile load (16,27). Our observation that cumulative transverse strain in healthy patellar tendons after exercise was also accompanied by concomitant increase in echo intensity (echogenicity), suggesting greater alignment or packing density of the solid phase of the tendon matrix after exercise, lends further support to this mechanism. It should be noted, however, that although quadriceps exercise resulted in similar (approximately 13%) increase in echogenicity (mean grayscale) in all tendons, the cumulative transverse strain response was markedly reduced in only the symptomatic tendon.

Previous research in animal models has demonstrated that tendon echogenicity is proportional to the applied load when tested in vitro (11,12). However, this relation has been shown to be highly nonlinear, with acoustic intensity approaching a plateau of around 12% with tensile stresses as low as 1.6 MPa (11). On the basis of previous studies and assuming a cross-section of approximately 100 mm2 (37), tensile stress in the human patellar tendon ranges between approximately 5 and 15 MPa during low-intensity physical activities such as walking and may reach up to approximately 30–40 MPa during high-intensity activities such as jumping (3,14). Increases in tendon echogenicity, therefore, would seem to occur at relatively low physiological loads. Thus, despite emerging evidence that the proximal patellar tendon may experience differential forces with mechanical loading (10), it would seem that the exercise protocol used in this study was sufficient to increase alignment of the solid phase of the matrix of the superficial and deep aspects of healthy and symptomatic patellar tendon, as evidenced by increase in echogenicity at both the proximal and mid-infrapatellar sites. Although alignment of the solid phase resulted in movement of interstitial fluid within the matrix of healthy tendons, as reflected by its transverse strain response, it was not sufficient to invoke fluid movement in symptomatic tendinopathy.

In the current study, patellar tendinopathy was characterized by a significantly thicker tendon in the symptomatic limb, which was accompanied by diffuse and focal areas of relatively low acoustic intensity involving the deep aspect of the infrapatellar tendon. Compared with that in healthy tendons, mean acoustic intensity was significantly lower in the superficial and deep aspects of both the symptomatic and asymptomatic patellar tendon. The finding suggests that morphological changes associated with tendinopathy may reflect a systemic or bilateral condition, as has been proposed with other “overuse” soft tissue injuries (46). In support of such a concept, strain-induced damage of the animal tendon has been shown to lower the intensity of acoustic echoes when imaged in vitro (12) and localization of focal hypoechoic regions to the deep surface of the patellar tendon is consistent with histological localization of pathology (collagen degradation and increased sulfated glycosaminoglycan deposition) in patellar tendinopathy (21). Collectively, these matrix disturbances may act to reduce fluid movement within the tendon by moderating the interstitial pressure associated with collagen realignment, lowering the permeability of the tendon matrix, and by increasing the proportion of bound water within the tendon matrix, thereby reducing the available amount of unbound water (45). Although reduced permeability associated with sulfated glycosaminoglycan deposition in the tendon is thought to maintain fluid pressure and increase compressive aggregate modulus, thereby protecting collagen fibers from further disruption (29), hydrostatic pressure and interstitial fluid movement are known to produce a wide range of phenomena in musculoskeletal tissues, including streaming potentials, lubrication, nutrient transport, and mechanical signaling, which are important in tissue differentiation and homeostasis (38). Given that interstitial fluid movement is thought to play a key role in mechanotransduction and tendon homeostasis (16), it may be speculated that diminished fluid movement with tendinopathy, as evidenced by lower transverse strain response to exercise, may contribute to the impaired capacity of the patellar tendon to adapt to mechanical loading in tendinopathy. In support of this concept, similar changes in tendon echotexture of the rotator cuff and impaired transverse strain response of the Achilles tendon to exercise have also been previously reported with clinical tendinopathy (5,15).

Consistent with previous research (44), we observed acute decrease in tendon thickness in healthy patellar tendon in response to exercise, equating to a cumulative transverse strain of approximately 6% in the healthy tendon. The magnitude of this creep response, however, was markedly less than that previously reported for healthy Achilles tendon (approximately 15%–20%) after intense resistance exercise (19,43,45) but was comparable with that reported for the Achilles tendons (approximately 5%) after 1 h of floorball match play (13). Direct comparisons between studies, however, are hampered by differences in study populations, the structure of the examined tendon and the loading protocols used. Nonetheless, the magnitude of dynamic creep in other soft tissues, such as the intervertebral disc, is thought to depend on the quantity of unbound fluid within the fluid flow pathway and marked changes in the creep behavior of the disc have been shown with manipulation of tissue hydration (41). Thus, the lower transverse creep observed in healthy patellar tendons in this study may partly reflect differences in unbound fluid between the Achilles and patellar tendon despite evidence that the total water content is similar between the two tendons (33). Previous research, however, has also demonstrated that the extent of axial creep in soft tissues is dependent on the magnitude and duration of the applied stress, with higher stresses eliciting greater creep response (39). Given that the ratio of the cross-sectional area of the Achilles tendon to the physiological cross-sectional area of the triceps surae (300–500) is 2–3 times that of the patellar tendon to quadri ceps surae (100–250), it is likely that average axial stress within the patellar tendon is typically less than that of the Achilles tendon during activities of daily living (40). It is noteworthy that the total loading impulse of the exercise protocol used in this study, however, is substantially lower (approximately half) than that used previously (43,45), with the total load and number of repetitions equating to only approximately 70% and 50% of that used in common eccentric rehabilitation protocols, in which 90 repetitions of unipedal loading has been advocated (35). Nonetheless, the exercise protocol in this study was sufficient to differentiate between individuals with and without tendinopathy and induced a similar magnitude of transverse strain at both the proximal (5 mm) and mid-infrapatellar (25 mm) tendon sites. This suggests that within a given tendon, the unbound fluid content, fluid pathway, and interstitial pressure are likely comparable and that exercise-induced transverse strains are relatively uniform across the measured tendon sites.

Although previous studies have shown that intratendinous Doppler flow can be present in both healthy and symptomatic patellar tendons (18), we observed no signs of microvascularity in healthy tendons with PDU. Thus, the cumulative transverse strain response of tendons to exercise is unlikely to be the result of a transient reduction in vascularity. However, six of the nine participants with patellar tendinopathy (67%) presented with neovascularization in the symptomatic tendon before exercise. Exercise resulted in significant (57% on average) reduction in PDU area in the current study (in five of the six participants) when measured immediately after exercise. This finding is consistent with the decrease in Doppler signal recently reported in Achilles tendinopathy when measurements were taken within 1 min of cessation of a calf raise exercise (31) but are in direct opposition to that noted by previous studies in which the postexercise ultrasound was deferred until 30–60 min after physical activity (4,22). This finding suggests that the magnitude of microvascularity in tendinopathy is related to loading history and highlights the importance of providing rest from physical activity immediately before sonographic imaging for detecting Doppler signal in the pathological patellar tendon. Interestingly, in our cohort, the postexercise decrease in PDU area was strongly and negatively correlated with self-reported symptom severity and accounted for 87% of the variance in the VISA-P score. Thus, at least in this relatively small sample, large reductions in PDU area after exercise were strongly associated with greater symptom severity or lower VISA-P scores. Although the relation between tendon pain and pathology is not straightforward and the present experimental setup does not allow for mechanistic explanation, it is possible that the reduction in microvascularity after exercise reflects greater hydrostatic pressure within tendon, resulting in relative hypoxia within neurovascular structures that in turn exacerbates painful symptoms. Although hypoxia has been implicated in the pathogenesis of tendinopathy and may stimulate neovascularization (1), the effect was not captured by the more commonly used qualitative scale (Öhberg score) (9). Although this may reflect the qualitative nature of the latter measure, it is noteworthy that three of nine participants with painful patellar tendinopathy in the current study had no observable microvascularity with PDU. Consequently, further prognostic studies involving larger cohorts are recommended to elucidate potential relations between the immediate postexercise change in Doppler flow and clinical symptoms in patellar tendinopathy.

This study evaluated the effect of tendinopathy on the cumulative transverse strain response of the patellar tendon immediately after resistance exercise that involved periodic concentric and eccentric modes of muscle contraction. Although there is evidence that both the type (eccentric/concentric) and duration of muscle contraction may influence blood flow and mechanical creep in the tendon (24,32), the magnitude of the acute mechanical response observed in the current study may not be transferable to other types and modes of exercise. A further limitation of this study is that we determined the strain response of the patellar tendon to exercise in only one dimension. Although there is evidence that mechanical properties of tendon are transversely isotropic (26) and that reductions in mediolateral tendon thickness, albeit in the Achilles, have also been observed with loading (19), it is unknown whether the effects of exercise result in comparable mediolateral strains in the patellar tendon. Similarly, we determined the response of the tendon to exercise at standardized distances (5 and 25 mm) from the inferior pole of the patella, rather than using a predefined percentage of total tendon length. Evaluating transverse strains at standard distances from the patellar pole does not account for variations in tendon length between groups. Although we found significant differences in height between our groups and a longer patellar tendon relative to the patella has been implicated in development of patellar tendinopathy (20), recent research using magnetic resonance imaging has reported no difference in tendon length between those with and without tendinopathy (36). Moreover, it should be recognized that patellar tendon length typically exceeds the footprint of most ultrasonic transducers and although alternative sonographic methods, including extended field of view and surface marker techniques, have been proposed, these techniques may introduce substantial (5%–35%) error in measures of tendon length (30,47). As such, we did not attempt to normalize our measurement location to tendon length, thereby avoiding the introduction of additional uncertainty into the data. Our observation that cumulative transverse strain was comparable at both the 5- and 20-mm measurement sites, however, would tend to suggest that exercise-induced transverse strain is relatively uniform across the proximal infrapatellar tendon.

Nonetheless, the findings of the current study suggest that patellar tendinopathy is associated with altered morphological and mechanical responses to exercise, which are primarily manifest by changes in cumulative transverse tendon strain. Structural changes associated with symptomatic tendinopathy would seem to minimize shear-induced fluid movement within the tendon matrix with mechanical loading and, when present, simultaneously lower microvascularity in the tendon. Altered microvascularity and diminished load-induced fluid movement, in turn, may disrupt mechanotransduction and homeostatic processes within the tendon and speculatively may contribute to the impaired adaptive capacity of the patellar tendon to exercise and underlie the progression of tendinopathy. In light of evidence that tendinopathy likely represents a continuum of disease progressing from reactive through degenerative stages (6), future research directed toward identifying both intrinsic (participant specific) and extrinsic (external loading) factors that influence the microvascular and cumulative transverse strain response of the patellar tendon to exercise in the various stages of tendinopathy is needed.

CONCLUSIONS

This is the first study to show that, in comparison with a healthy tendon, the immediate transverse strain response of the patellar tendon to exercise is diminished with tendinopathy. Given that interstitial fluid movement is thought to play a key role in convective transport, mechanotransduction, and tendon homeostasis, the acute transverse strain response of tendon to a defined exercise protocol may reflect the progression of patellar tendinopathy and may provide clinicians with an index for evaluating tendon resilience, which can be used to objectively monitor the progress of tendon rehabilitation programs. It is recommended that future research be directed toward exploring the immediate microvascular and cumulative strain responses of the patellar tendon to mechanical loading and their potential role in the progression of patellar tendinopathy.

The authors would like to thank Ms Melina Simjanovic and Ms Kristen Eales for their assistance with data collection.

This research was partly funded by the Australian Institute of Sport, Queensland Academy of Sport, Queensland government, and the Australian Research Council.

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.

REFERENCES

1. Alfredson H, Ohberg L, Forsgren S. Is vasculo-neural ingrowth the cause of pain in chronic Achilles tendinosis? An investigation using ultrasonography and colour Doppler, immunohistochemistry, and diagnostic injections. Knee Surg Sports Traumatol Arthrosc. 2003; 11: 334–3.
2. Arya S, Kulig K. Tendinopathy alters mechanical and material properties of the Achilles tendon. J Appl Physiol (1985). 2010; 108: 670–5.
3. Besier TF, Fredericson M, Gold GE, Beaupre GS, Delp SL. Knee muscle forces during walking and running in patellofemoral pain patients and pain-free controls. J Biomech. 2009; 42: 898–905.
4. Boesen AP, Boesen MI, Koenig MJ, Bliddal H, Torp-Pedersen S, Langberg H. Evidence of accumulated stress in Achilles and anterior knee tendons in elite badminton players. Knee Surg Sports Traumatol Arthrosc. 2011; 19: 30–7.
5. Collinger JL, Fullerton B, Impink BG, Koontz AM, Boninger ML. Validation of greyscale-based quantitative ultrasound in manual wheelchair users: relationship to established clinical measures of shoulder pathology. Am J Phys Med Rehabil. 2010; 89 (5): 390–400.
6. Cook JL, Purdam CR. Is tendon pathology a continuum? A pathology model to explain the clinical presentation of load-induced tendinopathy. Br J Sports Med. 2009; 43: 409–16.
7. Couppé C, Kongsgaard M, Aagaard P, et al. Habitual loading results in tendon hypertrophy and increased stiffness of the human patellar tendon. J Appl Physiol (1985). 2008; 105 (3): 805–10.
8. Couppe C, Kongsgaard M, Aagaard P, et al. Differences in tendon properties in elite badminton players with or without patellar tendinopathy. Scand J Med Sci Sports. 2013; 23: e89–95.
9. de Vos RJ, Weir A, Cobben LP, et al. The value of power Doppler ultrasonography in Achilles tendinopathy: a prospective study. Am J Sports Med. 2007; 35 (10): 1696–701.
10. Dillon EM, Erasmus PJ, Müller JH, Scheffer C, de Villiers RV. Differential forces within the proximal patellar tendon as an explanation for the characteristic lesion of patellar tendinopathy: an in vivo descriptive experimental study. Am J Sports Med. 2008; 36 (11): 2119–27.
11. Duenwald-Kuehl S, Kobayashi H, Frisch K, Lakes R, Vanderby R JrUltrasound echo is related to stress and strain in tendon. J Biomech. 2011; 44: 424–9.
12. Duenwald-Kuehl S, Lakes R, Vanderby R JrStrain-induced damage reduces echo intensity changes in tendon during loading. J Biomech. 2012; 45 (9): 1607–11.
13. Fahlström M, Alfredson H. Ultrasound and Doppler findings in the Achilles tendon among middle-aged recreational floor-ball players in direct relation to a match. Br J Sports Med. 2010; 44 (2): 140–3.
14. Finni T, Komi PV, Lepola V. In vivo human triceps surae and quadriceps femoris muscle function in a squat jump and counter movement jump. Eur J Appl Physiol. 2000; 83: 416–26.
15. Grigg NL, Wearing SC, Smeathers JE. Achilles tendinopathy has an aberrant strain response to eccentric exercise. Med Sci Sports Exerc. 2012; 44 (1): 12–7.
16. Hannafin JA, Arnoczky SP. Effect of cyclic and static tensile loading on water content and solute diffusion in canine flexor tendons: an in vitro study. J Orthop Res. 1994; 12: 350–6.
17. Helland CJ, Bojsen-Moller T, Raastad T, et al. Mechanical properties of the patellar tendon in elite volleyball players with and without patellar tendinopathy. Br J Sports Med. 2013; 47 (13): 862–8.
18. Hirschmüller A, Frey V, Konstantinidis L, et al. Prognostic value of Achilles tendon doppler sonography in asymptomatic runners. Med Sci Sports Exerc. 2012; 44 (2): 199–205.
19. Iwanuma S, Akagi R, Kurihara T, et al. Longitudinal and transverse deformation of human Achilles tendon induced by isometric plantar flexion at different intensities. J Appl Physiol (1985). 2011; 110 (6): 1615–21.
20. Johnson DP, Wakeley CJ, Watt I. Magnetic resonance imaging of patellar tendonitis. J Bone Joint Surg. 1996; 78-B: 452–7.
21. Khan KM, Bonar F, Desmond PM, et al. Patellar tendinosis (jumper’s knee): findings at histopathologic examination, US, and MR imaging. Victorian Institute of Sport Tendon Study Group. Radiology. 1996; 200: 821–7.
22. Koenig MJ, Torp-Pedersen S, Boesen MI, Holm CC, Bliddal H. Doppler ultrasonography of the anterior knee tendons in elite badminton players: colour fraction before and after match. Br J Sports Med. 2010; 44: 134–9.
23. Kongsgaard M, Qvortrup K, Larsen J, et al. Fibril morphology and tendon mechanical properties in patellar tendinopathy: effects of heavy slow resistance training. Am J Sports Med. 2010; 38 (4): 749–56.
24. Kubo K, Ikebukuro T, Yaeshima K, Kanehisa H. Effects of different duration contractions on elasticity, blood volume, and oxygen saturation of human tendon in vivo. Eur J Appl Physiol. 2009; 106 (3): 445–55.
25. Kubo K, Ikebukuro T, Yaeshima K, Yata H, Tsunoda N, Kanehisa H. Effects of static and dynamic training on the stiffness and blood volume of tendon in vivo. J Appl Physiol (1985). 2009; 106: 412–7.
26. Kuo PL, Li PC, Li ML. Elastic properties of tendon measured by two different approaches. Ultrasound Med Biol. 2001; 27 (9): 1275–84.
27. Lanir Y, Saland EL, Foux A. Physico-chemical and microstructural changes in collagen fibre bundles following stretch in-vitro. Biorheology. 1988; 25 (4): 591–603.
28. Lian OB, Engebretsen L, Bahr R. Prevalence of jumper’s knee among elite athletes from different sports: a cross-sectional study. Am J Sports Med. 2005; 33: 561–7.
29. Loboa EG, Wren TAL, Beaupré GS, et al. Mechanobiology of soft skeletal tissue differentiation—a computational approach of a fiber-reinforced poroelastic model based on homogeneous and isotropic simplifications. Biomech Model Mechanobiol. 2003; 2: 83–96.
30. Maganaris CN. Validity of procedures involved in ultrasound-based measurement of human plantarflexor tendon elongation on contraction. J Biomech. 2005; 38: 9–13.
31. Malliaras P, Chan O, Simran G, Martinez de Albornoz P, Morrissey D, Maffulli N. Doppler ultrasound signal in Achilles tendinopathy reduces immediately after activity. Int J Sports Med. 2012; 33 (6): 480–4.
32. Malliaras P, Kamal B, Nowell A, et al. Patellar tendon adaptation in relation to load-intensity and contraction type. J Biomech. 2013; 46: 1893–9.
33. Maynard JA, Pedrini VA, Pedrini-Mille A, Romanus B, Ohlerking F. Morphological and biochemical effects of sodium morrhuate on tendons. J Orthop Res. 1985; 3: 236–48.
34. Ohberg L, Lorentzon R, Alfredson H. Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc. 2001; 9 (4): 233–8.
35. Purdam CR, Jonsson P, Alfredson H, et al. A pilot study of the eccentric decline squat in the management of painful chronic patellar tendinopathy. Br J Sports Med. 2004; 38 (4): 395–7.
36. Shalaby M, Almekinders LC. Patellar tendinitis: the significance of magnetic resonance imaging findings. Am J Sports Med. 1999; 27: 345–9.
37. Svensson RB, Hansen P, Hassenkam T, et al. Mechanical properties of human patellar tendon at the hierarchical levels of tendon and fibril. J Appl Physiol (1985). 2012; 112: 419–26.
38. Swartz MA, Fleury ME. Interstitial flow and its effects in soft tissues. Annu Rev Biomed Eng. 2007; 9: 229–56.
39. Thornton GM, Shrive NG, Frank CB. Ligament creep recruits fibres at low stresses and can lead to modulus-reducing fibre damage at higher creep stresses: a study in rabbit medial collateral ligament model. J Orthop Res. 2002; 20: 967–74.
40. Vereecke EE, AJ C. The role of hind limb tendons in gibbon locomotion: springs or strings? J Exp Biol. 2013; 216: 3971–80.
41. Vresilovic EJ, Johannessen W, Elliott DM. Disc mechanics with trans-endplate partial nucleotomy are not fully restored following cyclic compressive loading and unloaded recovery. J Biomech Eng. 2006; 128 (6): 823–9.
42. Wall ME, Banes AJ. Early responses to mechanical load in tendon: role for calcium signaling, gap junctions and intercellular communication. J Musculoskelet Neuronal Interact. 2005; 5: 70–84.
43. Wearing SC, Grigg NL, Hooper SL, Smeathers Je. Conditioning of the Achilles tendon via ankle exercise improves correlations between sonographic measures of tendon thickness and body anthropometry. J Appl Physiol (1985). 2011; 110 (5): 1384–9.
44. Wearing SC, Hooper SL, Purdam C, et al. The acute transverse strain response of the patellar tendon to quadriceps exercise. Med Sci Sports Exerc. 2013; 45 (4): 772–7.
45. Wearing SC, Smeathers JE, Urry SR, et al. The time-course of acute changes in Achilles tendon morphology following exercise. In: Fuss FK, Subic A, Ujihashi S, editors. The Impact of Technology on Sport II. Singapore: Taylor and Francis; 2008; 65–8.
46. Wearing SC, Smeathers JE, Urry SR, Sullivan PM, Yates B, Dubois P. Plantar enthesopathy: thickening of the enthesis is correlated with energy dissipation of the plantar fat pad during walking. Am J Sports Med. 2010; 38: 2522–7.
47. Weng L, Tirumalai A, Lowery C, et al. US extended-field-of-view imaging technology. Radiology. 1997; 203: 877–80.
Keywords:

TENDON; REHABILITATION; ULTRASOUND; BIOMECHANICS; FLUID FLOW; COLLAGEN

© 2015 American College of Sports Medicine