This is the author’s version of a work that was submitted/accepted for pub-lication in the following source:

Wearing, Scott C., Locke, Simon, Smeathers, James E., & Hooper, SueL. (2014) Tendinopathy alters cumulative transverse strain in the patellartendon postexercise. Medicine and Science in Sports and Exercise. (InPress)

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c© Copyright 2014 American College of Sports Medicine

This is a non-final version of an article published in final form in Medicine& Science in Sports & Exercise: Post Acceptance: June 30, 2014 doi:10.1249/MSS.0000000000000417

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1

Tendinopathy alters cumulative transverse strain in the patellar tendon

post exercise

Original Article

Short Title: Transverse strain in patellar tendinopathy

Scott C. Wearing,1,2 Simon Locke,2

James E. Smeathers1 Sue L. Hooper,2 1 Institute of Health and Biomedical Innovation, Queensland University of Technology, Queensland,

Australia

2 Centre of Excellence for Applied Sport Science Research, Queensland Academy of Sport, Queensland,

Australia

Conflicts of Interest and Source of Funding: This research was part 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. * Correspondence, proof reading, and reprint requests to: Scott C. Wearing Institute of Health and Biomedical Innovation Queensland University of Technology 60 Musk Avenue, Kelvin Grove, Qld 4059 Australia t: +61 7 3138 6444 f: +61 7 3138 60330 e: s.wearing@qut.edu.au

2

ABSTRACT

Introduction. This research evaluated the effect of tendinopathy on the cumulative

transverse strain response of the patellar tendon to a bout of resistive quadriceps exercise.

Methods. Nine adults with unilateral patellar tendinopathy (age 18.2±0.7 years, height

1.92±0.06 m and weight 76.8±6.8 kg) and ten healthy adults free of knee pain (age 17.8±0.8

years, height 1.83±0.05 m and weight 73.2±7.6 kg) underwent standardised sagittal

sonograms (7.2–14 MHz linear–array transducer) of both patellar tendons immediately prior

and following 45 repetitions of a double–leg decline–squat exercise performed against a

resistance of 145% bodyweight. Tendon thickness was determined 5–mm and 25–mm distal

to the patellar pole. 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

echogenicity were calculated within the superficial and deep aspects of each tendon site from

gray–scale profiles. Intratendinous microvessels were evaluated using power Doppler

ultrasound.

Results. The cumulative transverse strain response to exercise in symptomatic tendinopathy

was significantly lower than that of asymptomatic and healthy tendon (P<.05). There was

also a significant reduction (57%) in the area of microvascularity immediately following

exercise (P=.05), which was positively correlated (r=0.93, P<.05) with VISA-P score.

Conclusions. This study is the first to show that patellar tendinopathy is associated with an

altered morphological and mechanical response of the tendon to exercise, which is manifest

by a reduction in cumulative transverse strain and microvascularity, when present. Research

directed toward identifying factors that influence the acute microvascular and transverse

strain response of the patellar tendon to exercise in the various stages of tendinopathy is

warranted.

3

KEYWORDS

TENDON; REHABILITATION; ULTRASOUND; BIOMECHANICS; FLUID FLOW;

COLLAGEN

4

INTRODUCTION

Paragraph Number 1 Patellar tendinopathy (jumper’s knee) is a common musculoskeletal

condition in elite athletes, with a 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 tendon,

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.

Paragraph Number 2 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 of three months duration (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). While these discrepancies may in part 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

5

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.

Paragraph Number 3 The purpose of this research, therefore, was to evaluate the effect of

tendinopathy on the 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 following exercise.

METHODS

Paragraph Number 4 Nine young adults with unilateral patellar tendinopathy and ten healthy

control adults who competed in Australian state or reserve league volleyball competitions

participated in the study. All participants were members of the Queensland Elite

Development Volleyball Program, were non–smokers, non–medicated and participated in the

same volleyball–specific training program which incorporated a minimum of 14 hours of

physical activity (skills development training, strength and conditioning and match play) per

week based on self–report. No participant reported a medical history of diabetes,

inflammatory joint disease, or familial hypercholesterolemia. All participants with patellar

tendinopathy presented with pain and a sensation of stiffness particularly at the onset of

loading activities, focal thickening of the involved tendon and unilateral symptoms of greater

than six weeks duration. 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 written informed consent to the procedures of the study, which received

6

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 (α = .05, β = .20) based on previously published data for human tendon (44).

Paragraph Number 5 All participants reported to the laboratory having abstained from

vigorous physical activity and consumption of alcohol in the previous 12 hours. 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).

Paragraph Number 6 Sonographic examination of the patellar tendon was undertaken by a

single operator using a 7.2–14 MHz multi–frequency 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 was evaluated by

undertaking repeated measurements of a standard calibration phantom (040GSE, CIRS,

Norfolk, Virginia, USA), 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-MHz). The 95% limits of agreement for repeated measures of

27 separate calibration monofilaments was ± 100 µm.

7

Paragraph Number 7 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, colour velocity of 3.1 cm.s-1, a region of interest (ROI) of 2.5

cm x 1.1 cm and with the colour 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).

Paragraph Number 8 Following pre–exercise 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 second period of ascent and 2 second period of

descent. Exercises were performed in a Smith machine with an Olympic bar weighted so as to

achieve an effective resistance of 145% bodyweight. All exercises were performed on a

standard 25° decline board. Longitudinal grayscale and Doppler sonograms were repeated

within one minute of completion of the quadriceps exercises. In total, the exercise protocol

took around six minutes to complete.

Data Reduction and Statistical Analysis

Paragraph Number 9 Sonographic images were exported in DICOM format and analyzed

using MATLAB software (MathWorks Inc., Natick, MA, USA). 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–mm and 25–mm distal to the attachment at the

inferior pole of the patella (Figure 1a). Transverse Hencky strain (%) was calculated as the

natural log of the ratio of post– to pre–exercise tendon thickness and expressed as a

8

percentage. The within–subject coefficient of variation for repeated measurements of

transverse strain in the patellar tendon was 2.1%.

< Figure 1a & b about here>

Paragraph Number 10 Tendon echogenicity in the superficial and deep aspects of the

patellar tendon were 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 digitised superficial and deep tendon

borders. The ROI at each site was subsequently bisected to form an equally sized deep (D)

and superficial (S) 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 (Figure 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 there is a difference in the strains

experienced between the posterior fibres of the tendon and those of the anterior region (10).

Grayscale values within the ROIs ranged between zero and 255, with higher values indicative

of an hyperechoic tendon. The coefficient of variation for repeated measures of tendon

echogenicity was 5.5%.

Paragraph Number 11 Intratendinous power Doppler flow (PDU) was qualitatively graded

from 0 to IV using the modified Öhberg score (9, 34). In brief, tendons were scored as 0

when no vessels were visible, and I to IV when one to four or more vessels were visible

9

within the 2.5 cm x 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 colour pixels within the

tendon and the square of effective pixel resolution (Figure 1b,c). The limits of agreement for

repeated measurements of PDU area was ± 0.6 mm2.

Paragraph Number 12 The Statistical Package for the Social Sciences (SPSS Inc, Chicago,

IL, USA) 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 standard deviations 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 a within-subjects factors, while 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 a three–way repeated measures ANOVAs 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 ANOVAs in combination with Tukey’s post hoc analysis.

Differences in qualitative grade of neovascularization following exercise were evaluated

using a Wilcoxon Signed Ranks Test, while differences in PDU area were assessed using a

paired t-test. Potential relationships between PDU area and symptom severity (VISA-P

10

scores) were evaluated using Pearson product-moment correlations. An alpha level of .05 was

used for all univariate tests of significance.

RESULTS

Paragraph Number 13 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 =.002).

< Position Table 1 about here>

Paragraph Number 14 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 a significant interaction

between site and limb for measures of tendon thickness (F = 7.5, P = .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 < .05) and distal (F = 4.9, P < .05)

measurement sites (Figure 2). Repeated measures ANOVA also identified a significant

interaction between tendon region and limb for measures of average grayscale (F = 2.8, P=

.05). Post hoc analysis demonstrated that tendon echogenicity was significantly lower in the

deep, rather than superficial, region of symptomatic and asymptomatic patellar tendons when

compared with healthy controls at the proximal (F = 4.4, P < .05) measurement site (Figure

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

prior to exercise, with a median of IV. PDU area at baseline was moderately correlated with

11

VISA-P score (r = =-.58, P = .05), such that greater PDU area prior to exercise was associated

with lower (worse) symptom severity scores. Microvascularity was not present in tendons of

healthy participants.

< Position Figures 2 about here>

Paragraph Number 15 Exercise resulted in an immediate decrease in patellar tendon

thickness in healthy tendon at both proximal and distal measurement sites, which equated to a

cumulative transverse strain of approximately 6% (Figure 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 < .001). Post hoc analysis revealed that cumulative transverse strain was

significantly lower in symptomatic tendon than asymptomatic and healthy tendon (P <.05).

< Position Figure 3 about here>

Paragraph Number 16 As shown in Figure 3, there was a significant main effect of exercise

on tendon grayscale (F = 28.8, P < .001) with an increase in tendon echogenicity occurring

following exercise. In addition, exercise resulted in a significant reduction in PDU area in

those with PDU signal; decreasing by 57%, from 9.3 ± 8.3 mm2 prior to exercise to 5.3 ± 7.2

mm2 immediately post–exercise (t = 2.0, P = .05). As shown in Figure 5, post–exercise

change in PDU area was positively correlated (r = 0.93, P = .008) with VISA-P score, such

that greater post-exercise 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 post-exercise I,

range 0–IV, Z=-1.633, P=.102).

12

< Position Figure 4 & 5 about here>

DISCUSSION

Paragraph Number 17 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 tendon exposed to tensile load (16,

27). Our observation that cumulative transverse strain in healthy patellar tendon post–

exercise was also accompanied by a concomitant increase in echo intensity (echogenicity),

suggesting a greater alignment or packing density of the solid phase of the tendon matrix post

exercise, lends further support to this mechanism. It should be noted, however, that although

quadriceps exercise resulted in a similar (≈13%) increase in echogenicity (mean grayscale) in

all tendons, the cumulative transverse strain response was markedly reduced in only the

symptomatic tendon.

Paragraph Number 18 Previous research in animal models has demonstrated that tendon

echogenicity is proportional to the applied load when tested in vitro (11, 12). However, this

relationship has been shown to be highly non–linear, with acoustic intensity approaching a

plateau of around 12% with tensile stresses as low as 1.6 MPa (11). Based on previous

studies and assuming a cross–section of ≈100 mm2 (37), tensile stress in the human patellar

tendon ranges between about 5 and 15 MPa during low intensity physical activities such as

walking and may reach up to ≈ 30–40 MPa during high intensity activities such as jumping

13

(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 appear 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 an 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 tendon, as reflected by its transverse strain response, it was not sufficient to

invoke fluid movement in symptomatic tendinopathy.

Paragraph Number 19 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 healthy tendon, 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 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 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

14

the available amount of unbound water (45). Although reduced permeability associated with

sulfated glycosaminoglycan deposition in tendon is thought to maintain fluid pressure and

increase compressive aggregate modulus, thereby protecting collagen fibres 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 a 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 an impaired transverse strain response of the Achilles

tendon to exercise have also been previously reported with clinical tendinopathy (5, 15).

Paragraph Number 20 Consistent with previous research (44), we observed an acute

decrease in tendon thickness in healthy patellar tendon in response to exercise, equating to a

cumulative transverse strain of ≈6% in healthy tendon. The magnitude of this creep response,

however, was markedly less than that previously reported for healthy Achilles tendon (≈15–

20%) following intense resistance exercise (19, 43, 45), but was comparable to that reported

for the Achilles tendon (≈5%) after 1 hour of floor–ball match play (13). Although direct

comparisons between studies is hampered by differences in study populations, the structure

of the examined tendon and loading protocols employed, 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

15

transverse creep observed in healthy patellar tendon in this study may, therefore, 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 a greater creep

response (39). Given the ratio of the cross sectional area of the Achilles tendon to the

physiological cross-sectional area of the Triceps Surae (300–500) is two to three times that of

the patellar tendon to Quadriceps 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 about 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.

Paragraph Number 21 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 tendon with PDU. Thus, the cumulative transverse strain

response of tendon 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

16

with neovascularization in the symptomatic tendon prior to exercise. Exercise resulted in a

significant (57% on average) reduction in PDU area in the current study (in five of the six

participants) when measured immediately following exercise. This finding is consistent with

the decrease in Doppler signal recently reported in Achilles tendinopathy when

measurements were taken within one minute of cessation of a calf–raise exercise (31), but are

in direct opposition to that noted by previous studies in which the post–exercise ultrasound

was deferred until 30–60 minutes 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 prior to sonographic imaging

for detecting Doppler signal in pathological patellar tendon. Interestingly in our cohort, the

post–exercise 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 post exercise were

strongly associated with greater symptom severity or lower VISA–P scores. Although the

relationship between tendon pain and pathology is not straightforward and the present

experimental setup does not allow for a mechanistic explanation, it is possible that the

reduction in microvascularity following exercise reflects a greater hydrostatic pressure within

tendon resulting in relative hypoxia within neurovascular structures that in turn exacerbates

painful symptoms. While hypoxia has been implicated in the pathogenesis of tendinopathy

and may stimulate neovascularisation (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

17

elucidate potential relationships between the immediate post–exercise change in Doppler

flow and clinical symptoms in patellar tendinopathy.

Paragraph Number 22 This study evaluated the effect of tendinopathy on the cumulative

transverse strain response of the patellar tendon immediately following resistance exercise

that involved periodic concentric and eccentric modes of muscle contraction. While there is

evidence that both the type (eccentric/ concentric) and duration of muscle contraction may

influence blood flow and mechanical creep in 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 if the effects of exercise result in comparable mediolateral strains in the

patellar tendon. Similarly, we determined the response of tendon to exercise at standardized

distances (5 and 25 mm) from the inferior pole of the patella, rather than using a pre–defined

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 employing 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%)

18

error in measures of tendon length (30, 47). As such, we did not attempt to normalise 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–mm and 20–mm measurement sites, however, would tend to suggest that

exercise–induced transverse strain is relatively uniform across the proximal infrapatellar

tendon.

Paragraph Number 23 Nonetheless, the findings of the current study suggest that patellar

tendinopathy is associated with an altered morphological and mechanical response to

exercise, which is primarily manifest by changes in cumulative transverse tendon strain.

Structural changes associated with symptomatic tendinopathy would appear to minimise

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.

CONCLUSION

Paragraph Number 24 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

19

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 response of the patellar tendon to mechanical loading

and their potential role in the progression of patellar tendinopathy.

20

ACKNOWLEDGEMENTS

This research was part funded by the Australian Institute of Sport, Queensland Academy of

Sport, Queensland Government and the Australian Research Council. The authors would like

to thank Ms Melina Simjanovic and Ms Kristen Eales for their assistance with data

collection. The authors declare no conflicts of interest, financial or otherwise. The results of

the present study do not constitute endorsement by American College of Sports Medicine.

21

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FIGURE LEGENDS

Figure 1. Patellar tendon thickness was measured 5 mm (L1) and 25 mm (L2) inferior to the

patella pole (P) with the aid of a grayscale profile. At each site, average grayscale in the

superficial (S1, S2) and deep (D1, D2) aspects of the tendon were determined (a). Illustration

of the intratendinous power Doppler flow (PDU) within a 2.5 cm x 1.1 cm region of interest

that was graded using the modified Öhberg score (b). The area of the same intratendinous

PDU flow was also quantified by determining the number of colour 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).

Figure 2. Patellar tendon thickness in symptomatic, asymptomatic and left and right control

limbs measured 5 mm (Site 1) and 25 mm (Site 2) inferior to the patella pole. † Statistically

significant main effect for site (P < .05). * Significantly different from all other limbs at the

given site (P < .05).

Figure 3. Mean grayscale in the superficial and deep aspects of the patellar tendon prior to

(pre) and following (post) exercise in symptomatic, asymptomatic and left and right control

limbs and determined at two sites; 5–mm distal to the inferior pole of the patellar (a) and 25–

mm distal to the inferior pole of the patellar (b). Note that while average grayscale was

significantly lower in both symptomatic and asymptomatic tendon, there was a statistically

significant main effect for exercise in all tendons (P<.05).

Figure 4. Cumulative transverse strain in the patellar tendon in symptomatic, asymptomatic

and control limbs following exercise. Strain was determined 5 mm (site 1) and 25 mm (site 2)

28

distal to the inferior pole of the patella. * Significantly different from all other limbs at the

given site (P<.05).

Figure 5. The relationship between symptom severity (VISA-P) and change in PDU area in

the infrapatellar tendon immediately following exercise.