Sports Med DOI 10.1007/s40279-014-0201-y

REVIEW ARTICLE

Region-Specific Tendon Properties and Patellar Tendinopathy: A Wider Understanding Stephen John Pearson • Syed Robiul Hussain

Ó Springer International Publishing Switzerland 2014

Abstract Patellar tendinopathy is a common painful musculoskeletal disorder with a very high prevalence in the athletic population that can severely limit or even end an athletic career. To date, the underlying pathophysiology leading to the condition remains poorly understood, although reports suggesting that patellar tendinopathy most frequently concerns the proximal posterior region of the tendon has prompted some researchers to examine regionspecific tendon properties for a better understanding of the etiology and potential risk factors associated with the condition. However, to date, research concerning the in vivo region-specific tendon properties in relation to patellar tendinopathy is very scarce, perhaps due to the lack of validated techniques that can determine such properties in vivo. In recent years, a technique has been developed involving an automated tendon-tracking program that appears to be very useful in the determination of regionspecific tendon properties in vivo. In terms of regional variations in tendon properties, previous research has demonstrated differences in structural, mechanical, and biochemical properties between the discrete regions of the patellar tendon, but the extent to which these regional variations contribute to patellar tendinopathy remains elusive. In addition, with respect to treatment strategies for patellar tendinopathy, previous research has utilized a wide range of interventions, but the use of eccentric exercise (EE) and/or heavy-slow resistance (HSR) training appear to be most promising. However, the optimal program design variables of EE and HSR training that induce the most favorable effects are yet to be determined. This review S. J. Pearson (&)
S. R. Hussain Centre for Health, Sport and Rehabilitation Sciences Research, University of Salford, Manchester M6 6PU, UK e-mail: [email protected]

article provides a detailed discussion of all of the above to allow a better understanding of the etiology and potential risk factors associated with the condition as well as the most effective treatment strategies. First, a comprehensive literature review is provided with respect to region-specific structural, mechanical, and biochemical properties, in association with patellar tendinopathy. Second, the automated tendon-tracking methodology is outlined to assist future researchers in the determination of region-specific tendon properties. Finally, potential treatment strategies are discussed, particularly with regards to the use of EE and HSR training for the management of patellar tendinopathy.

1 Background Patellar tendinopathy is a common degenerative musculoskeletal disorder that affects athletes in a wide range of sports, particularly those associated with explosive jumping [1–3]. For instance, its prevalence has been reported to be 44.6 % in elite volleyball players [2] and 31.9 % in elite basketball players [3]. Hence, it is also commonly described as ‘jumper’s knee’, although this term should be used cautiously as it can refer to problems with both the quadriceps tendon (proximal to patellar) and the patellar tendon (distal to patellar) [3]. However, for clarification purposes, ‘jumper’s knee’ refers specifically to patellar tendinopathy in this article. Jumping activities, in particular, appear to impose considerable forces on the knee extensor mechanism [4, 5], and although the etiology of patellar tendinopathy remains elusive, the magnitude of loading on the patellar tendon has been suggested to be an important causative factor [4, 6, 7]. More specifically, the magnitude of patellar tendon loading appears to be associated with jumping technique, in that the

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large external tibial torsional moment during take-off [4], and increased ankle dorsiflexion and trunk flexion [7] as well as deep knee flexion [4] during landing, have been reported to predispose the patellar tendon to great forces, ultimately increasing risk of developing patellar tendinopathy. Patellar tendinopathy is associated with many degenerative changes, including the absence of inflammatory cells in the tendon, a tendency toward poor healing, and decreased quality and disorganization of collagen fibers, all of which may lead to decreased tensile strength [8]. This can severely limit or even end an athletic career. It has been suggested that up to one-third of patients will have significant pain and functional limitation at 6 months following the onset of symptoms and, for the majority, some level of symptoms will persist for many years [9]. A prospective case–control study by Kettunen et al. [10] also showed the long-term outcome (15 years) of athletes with jumper’s knee. Here, 53 % of subjects (9 of 17) had to end their sports career due to the condition [10]. Despite its high prevalence and therapeutically challenging nature, the pathomechanics of patellar tendinopathy remain largely unknown. It has been suggested that the pathological tendon changes in patellar tendinopathy are typically located in the posterior proximal tendon at the insertion on the deep aspect of the patellar bone [11, 12]. Khan et al. [12] demonstrated marked histopathological changes in the proximal patellar tendon accompanied by clear abnormalities in the same location with magnetic resonance imaging and ultrasonography. This could possibly be attributed to variations in intra-tendinous loading patterns, since studies have demonstrated that the anterior and posterior aspects of the human patellar tendon are exposed to different magnitudes of tensile strain during knee flexion [13, 14]. In addition, a study on isolated tendon fascicles taken from the anterior and posterior regions of the patellar tendon showed lower tensile strength in the posterior fascicles [15]. Thus, it is possible that such variations in loading patterns [13, 14] correlate to regional differences in mechanical properties within the patellar tendon [15]. In support of this, Lavagnino et al. [16] also demonstrated increased localized tendon strain at the classic lesion site of ‘jumper’s knee’ (proximal posterior tendon). Collectively, previous research appears to support the idea that the underlying pathophysiology of patellar tendinopathy is related to differential intra-tendinous loading patterns and regional variations in mechanical properties. It is possible to determine the mechanical properties of the tendon through the combined use of dynamometry (to record joint torques), electromyography (to account for antagonist co-contraction torque), magnetic resonance imaging (to determine tendon moment arm length), and

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B-mode linear ultrasound imaging (to record tendon excursion/displacement) during ramped isometric loading conditions [17–22]. Previous research also indicates that tendinopathy may alter the structural and mechanical properties of the tendon [23–25]. Helland et al. [23] reported a group of elite volleyball players with patellar tendinopathy to exhibit significantly lower tendon stiffness (mean ± standard deviation [SD] 2,254 ± 280 vs. 2,826 ± 603 N
mm-1) and Young’s modulus (mean ± SD 0.99 ± 0.16 vs. 1.17 ± 0.25 GPa), but a larger proximal tendon crosssectional area (CSA) (mean ± SD 133 ± 11 vs. 112 ± 9 mm2), relative to healthy matched controls. Couppe´ et al. [24] also reported greater tendon stress (mean ± SD 32 ± 3 vs. 21 ± 3 MPa) in a cohort of elite badminton players with patellar tendinopathy than in those not afflicted with the condition. Moreover, a study examining the Achilles tendon also found tendinopathic tendons to display greater CSA and lower values of stiffness and Young’s modulus than those without tendinopathy [25]. Based on these considerations, it appears that increased tendon CSA with reduced tendon stiffness and Young’s modulus are found with tendinopathy. Indeed, the reduced stiffness and Young’s modulus may present a disadvantage in terms of muscle function and injury risk. A less stiff tendon would not only compromise the rate of force development [26], which is an important determinant of performance for explosive jumping athletes, but would also lend itself to greater tendon deformation for equivalent forces, thus increasing the risk of potential strain-related injuries [27]. Although previous investigations have provided an insight into tendon properties associated with tendinopathy, as well as the potential functional deficits, their principal focus has been to examine the tendon structure as a whole. As such, they do not provide any information in terms of how each discrete region of the patellar tendon may be modulated with the condition. Given that patellar tendinopathy is typically region specific [11, 12], this appears to be a very important consideration, with region-specific mechanical properties enabling a more complete characterization of the tendon. However, to date, there has been a lack of validated techniques that can determine such properties in vivo, which in turn has limited the research in this area. In recent years, a technique has been established that allows the assessment of region-specific mechanical properties of human tendons in vivo [28]. This technique is similar to the traditional methods as previously outlined [17–22], with the addition of an automated tendon tracking (speckle tracking) program to determine regional differences in strain patterns. Previous research has also validated [28] and utilized this method to determine the in vivo

Region-Specific Tendon Properties and Patellar Tendinopathy

mechanical properties of human tendons with respect to specific regions [29, 30]. However, the scientific literature currently lacks a review article on region-specific tendon properties in relation to patellar tendinopathy, which is warranted in order to achieve a more complete understanding of the pathomechanics that lead to the condition, as well as the potential risk factors and most effective treatment strategies. Thus the purpose of this review is to (1) provide a review of the literature with respect to regionspecific tendon properties, in association with patellar tendinopathy, (2) outline the automated tracking method as used by recent studies for the determination of regionspecific mechanical properties to inspire future research, and (3) discuss potential treatment strategies for the management of patellar tendinopathy.

2 Literature Search Methodology The National Library of Medicine (PubMed) database was used to search for all articles used in this review. The specific search terms used were ‘patellar tendinopathy’, ‘patellar tendinitis’, ‘jumper’s knee’, ‘patellar tendon’, ‘tendon injury’, ‘region specific tendon properties‘, ‘mechanical properties’, ‘tendon strain’, and ‘treatment’. Reference lists of articles obtained from this search were also examined for additional relevant articles. The inclusion criteria were based on potential relevance with regards to patellar tendinopathy and/or tendon properties.

3 Region-Specific Tendon Properties and Patellar Tendinopathy The following sections relate to aspects of tendon properties examined between different regions of the intact tendons, emphasizing regional differences in structural, mechanical, and biochemical properties, and their relationship to patellar tendinopathy (if any). 3.1 Structural Properties It is evident that tendon CSA differs throughout the length of the tendon structure [31–33]. For instance, Kongsgaard et al. [32] reported the CSA of the patellar tendon to be smallest at the proximal region (mean ± SD 104 ± 4 mm2) and largest at the distal region (mean ± SD 127 ± 2 mm2) (P \ 0.05). This is also supported by Couppe´ et al. [33], where the patellar tendon CSA was again greater at the distal than at the middle and proximal regions (P \ 0.05). Collectively, previous research supports the view that CSA of the patellar tendon is typically greatest at the distal region and smallest at the proximal.

However, it must be noted that these studies were not carried out on patellar tendinopathy patients and as such do not reflect the specific regional structural characteristics associated with the condition. To date, it is not well understood how each discrete region of the patellar tendon is structurally modulated with tendinopathy. However, previous research does suggest that the structural changes are most frequently associated with the proximal posterior region of the tendon [11, 12, 23, 34]. Through the use of magnetic resonance imaging and ultrasound, Khan et al. [12] reported distinct histopathological changes with clear abnormalities specifically in the proximal region of the patellar tendon in a cohort of athletes with jumper’s knee. In addition, Johnson et al. [11] reported a significant thickening of the tendon that was most common in the posterior proximal aspect in a group of patellar tendinitis patients. This is also consistent with the case–control studies of Helland et al. [23] and Lian et al. [34], where a greater tendon CSA at the proximal region and a larger anteroposterior thickness were demonstrated in a cohort of elite volleyball players with patellar tendinopathy compared with healthy matched controls. Furthermore, image findings with color Doppler examination have shown the presence of neovascularization with structural tendon changes mainly in the proximal patellar tendon [35, 36]. Therefore, based on these studies, it appears that the structural tendon changes with patellar tendinopathy are particularly associated with the proximal posterior region of the tendon. However, the etiology of this is unclear, although it may perhaps relate to intratendinous variations in the magnitude of loading found during contractile activity [13, 14], which may predispose certain regions of the tendon to greater injury risk. It must also be noted that these studies are retrospective and most have not fully quantified the structural properties of tendinopathic tendons in the sense of length and CSA. This could prove particularly useful for clinicians with regards to normative data, ultimately improving diagnosis and clinical knowledge. Thus, more research is needed to accurately determine the region-specific structural properties associated with patellar tendinopathy. However, based on the current research, it appears that patellar tendon CSA may be increased with tendinopathy, particularly in the proximal posterior region. Although Couppe´ et al. [24] reported the opposite in that subjects with patellar tendinopathy were found to display a smaller tendon CSA, these researchers principally focused on assessing the distal aspect of the patellar tendon, which may explain their contrasting findings, as the changes in patellar tendinopathy most frequently concern the posterior proximal region [11, 12]. The reports of increased tendon CSA with patellar tendinopathy are also consistent with data on Achilles tendinopathy [25, 37, 38], and could

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perhaps be due to the accumulation of water and increased ground substance as a result of the pathology [39]. Although a larger tendon is generally considered mechanically stronger due to its ability to dissipate high stresses (force/area) across the tendon and yield lower strain energy, the study of Helland et al. [23] demonstrated that, despite having a greater CSA, the tendinopathic patellar tendons exhibited lower values of stiffness and Young’s modulus than did healthy tendons. Similar results have also been shown in tendinopathic Achilles tendons with respect to increased CSA and reduced stiffness and Young’s modulus [25]. This is most likely a result of the alterations in intrinsic tendon tissue composition and arrangement accompanying the degenerative process, thereby subjecting the tendon to higher degrees of strain despite having a greater CSA. The specific changes in the tendon matrix with tendinopathy may include a separation and loss of type I collagen fibers, loss of transverse bands of collagen fibers, increased collagen fiber crimping and ruptures, and increased production of mechanically weaker type III collagen [40]. All of these structural and compositional changes may adversely affect the tendon’s mechanical properties, thus predisposing the individual to impaired muscle function and further injury risk. 3.2 Mechanical Properties A number of studies have reported differences in mechanical properties between the discrete regions of the tendon [13–15, 29, 30]. Based on these, it is evident that tensile strain throughout the tendon structure is not equal for a given external force, perhaps due to differences in collagen cross-linking [41], fibril morphology [42–44], and components of the extracellular matrix [45, 46] between the different regions of the tendon, leading to potential regional variations in mechanical properties. Additionally, lever arm differences, which can be seen for the patellar tendon, may also partly contribute to the regional variation in mechanical properties. In other words, the lever arm advantage is greater on the anterior region than on the posterior for the proximal tendon. Thus, all factors being equal, the proximal posterior region of the tendon may in fact be ‘stress shielded’, a theory demonstrated by Yamamoto et al. [47]. Indeed, the observed regional differences in strain may indicate an increased risk for injury in certain areas of the tendon, which may also lend some perspective to the development of patellar tendinopathy, as this condition most frequently concerns the posterior proximal aspect of the tendon [11, 12, 48]. However, there is currently a lack of evidence concerning regional differences of the patellar tendon in vivo. An in vitro study by Basso et al. [14] found quadriceps loading of cadaver knees in flexion to induce

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greater strain on the posterior than on the anterior side of the patellar tendon, thus supporting the tensile-overload theory, whereby potential posterior tendon overuse may lead to patellar tendinopathy. Through the use of an optic fiber technique, Dillon et al. [49] also reported similar findings in that tendinous forces are greater in the posterior region of the patellar tendon relative to the anterior region during quadriceps loading. However, these findings are sharply contrasted by Almekinders et al. [13], who reported tensile strain to increase on the anterior side and decrease on the posterior as the knee was brought into flexion in human cadaver knees, suggesting that the posterior portion of the tendon may not be subjected to the highest tensile loads in the functional flexion range and are, consequently, stress shielded. These findings, contrasting with those of Basso et al. [14], could in part be due to methodological differences, since Basso et al. [14] utilized a greater knee flexion angle (90° vs. 60°) than that of Almekinders et al. [13]. The authors then concluded that stress shielding may play a more important role in the etiology of patellar tendinopathy as opposed to repetitive tensile loading [13]. This suggestion is also supported by studies on isolated tendon fascicles extracted from the anterior and posterior regions of the patellar tendon [15, 50]. Anterior fascicles have previously been reported to be markedly stronger and stiffer [50], and also to display significantly greater peak and yield stress, and tangent modulus [15] than posterior fascicles. These studies may suggest that the anterior region of the patellar tendon has adapted to its level of mechanical usage, perhaps due to a repeated exposure to high tensile loads and thus is able to withstand high magnitudes of tensile strain, leaving the posterior and weaker part of the tendon more susceptible to strain-related injury (stress shielded). Thus, the currently available data on region-specific mechanical properties of the patellar tendon are sparse and conflicting [13–15, 50], and more importantly are mainly based on either older cadaver specimens (mean 59 and 73 years) or isolated tendon fascicles obtained from different regions, which may not necessarily reflect the characteristics of the whole discrete regions of the human patellar tendon functioning in vivo. However, to date, no data exist on the in vivo region-specific mechanical properties of the patellar tendon. It is also notable that previous research has not yet determined the region-specific mechanical properties of the patellar tendon in patellar tendinopathy patients, and so, the above-reported findings may not necessarily reflect the specific regional characteristics associated with the condition. This is indeed an area that requires further research so that normative data are made available to allow clinicians to have a reference point for comparison in the clinical context and to enable effective treatment to be optimized.

Region-Specific Tendon Properties and Patellar Tendinopathy

3.3 Biochemical Properties At the cellular level, tendons are primarily composed of type I collagen fibrils, which are thought to be major loadbearing units of the tendon [51]. The mechanical integrity of fibrils is believed to be augmented by so-called ‘mature’ cross-links [51, 52]. Mature cross-links are trivalent chemical bonds that link neighboring collagen molecules together and strengthen the collagen lattice [51]. Immature enzymatically derived cross-links spontaneously convert into the trivalent form with maturation [53]. In human tendons, the pyridinium type cross-links lysylpyridinoline (LP) and hydroxylysylpyridinoline (HP) constitute such mature cross-links [53, 54]. Additionally, non-enzymatic glycation of collagen occurs with aging, leading to the accumulation of advanced glycation end-products (AGEs), which further cross-link the collagen molecules and lead to a stiffer and more load-resistant tendon. The most widely studied AGE is pentosidine, which is commonly used as a biomarker of non-enzymatic glycation [53, 54]. To the authors’ knowledge, only one previous study has attempted to explore the variation in biochemical properties between different regions of the tendon in humans [50]. The study by Hansen et al. [50] on isolated tendon fascicles examined differences in mechanical properties as well as fibril morphology and biochemical cross-link composition (HP, LP, AGE, pentosidine) between the anterior and posterior regions of the patellar tendon. Tendon fascicles were obtained from elective anterior cruciate ligament (ACL) surgery patients and tested micromechanically. The results showed anterior fascicles to be markedly stronger (mean ± SD 54.3 ± 21.2 vs. 39.7 ± 21.3 MPa, P \ 0.05) and stiffer (mean ± SD 624 ± 232 vs. 362 ± 170 MPa, P \ 0.01) than posterior fascicles. The reduced strength of the posterior fascicles was also accompanied by more densely packed fibrils, with smaller fibril diameters that displayed a tendency towards smaller CSAs (mean ± SD 7.819 ± 2.168 vs. 4.897 ± 1.434 mm2), which corresponds well with previous reports, as smaller fibrils are generally thought to be weaker [42]. Collectively, the study’s data on mechanical properties and fibril morphology suggest that the posterior region of the tendon may be stress shielded, thus agreeing with the in vitro study by Almekinders et al. [13]. Biochemically, AGE concentration as represented by pentosidine, was similar in the anterior and posterior regions. However, quite surprisingly, the concentration of mature HP and LP cross-links was greater in the posterior and weaker part of the patellar tendon (HP mean ± SD 0.859 ± 0.197 vs. 1.416 ± 0.250 mol/mol, P \ 0.001; LP mean ± SD 0.023 ± 0.006 vs. 0.035 ± 0.006 mol/mol, P \ 0.01), which contradicts the general notion that collagen cross-link concentration is positively related to the

strength of collagen tissues [53–55]. This perhaps suggests that other factors also contribute to tendon strength. One such factor could be the putative inter-fibrillar pyrrole cross-link, which has previously been associated with strength of cortical bone [56], but so far has not been explored in relation to tendon function and mechanics. Ultimately, the study showed that variations in mechanical properties between the anterior and posterior regions of the patellar tendon are not associated with alterations in biochemical composition. Interestingly, however, based on these findings, it appears that the posterior region of the patellar tendon exhibits similar characteristics to ligaments in terms of fibril morphology and biochemical composition [57–59]. Therefore, perhaps the human patellar tendon should be regarded as two distinct functional units, an anterior tendon unit and a posterior ligament unit. Anatomically, the posterior portion of the patellar tendon connects the patellar sesamoid bone to the tibial tuberosity, whereas the anterior portion appears as a continuity of the quadriceps tendon. Furthermore, compared with tendons, ligaments have increased concentration of the immature cross-link dihydroxylysinonorleucine (DHLNL) (a precursor of HP [57]), a higher concentration of pyridinoline [59], and a larger number of small fibrils [58], which is in line with the findings of Hansen et al. [50]. However, this is beyond the scope of this review to determine and thus requires further research.

4 Automated Tendon-Tracking Methodology The lack of research on region-specific tendon properties has limited the understanding of the etiology and potential risk factors associated with patellar tendinopathy. The primary purpose of this section is to outline the automated tendon-tracking methodology with respect to mechanics and validity to assist and/or inspire future research in determining region-specific tendon properties for a better understanding of the topic. 4.1 Mechanics Automated tendon tracking typically involves the use of a block matching algorithm with normalized cross-correlation (NCC), which is then used to track the different regions of the tendon [28]. Briefly, multiple search blocks (or regions of interest) are placed on the different layers of the tendon (anterior, mid, posterior) in the proximal and distal aspects. The search blocks are then utilized to track their associated tendon region from the start to end points, and essentially calculate tendon excursion for each discrete region of the tendon at any given level of muscle force (see Fig. 1).

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Fig. 1 A typical illustration of patellar tendon excursion during a ramped isometric knee extension. Tendon strain can be determined for each discrete region of the tendon via the use of automated tendon tracking. Two search blocks or regions of interest (R1 and R2) are placed in the anterior (layer 1), mid (layer 2), and posterior (layer 3) regions of the tendon in the proximal (a) and distal (b) aspects. R1

and R2 then track their corresponding tendon region from the start (rest) to end (100 % force) points. The red/purple squares here represent the moved regions from start (grey squares). Percent strain is then determined as change in length/original length 9 100. Regional strain differences can then be determined by comparison of strain values

4.2 Validity

5 Conservative Treatment Strategies

Previous research has also studied the validity of the automated tracking method for estimation of tendon movements in vivo [28, 60–62]. Korstanje et al. [60] reported minor errors of 1.6 % (mean) when attempting to track the flexor digitorum superficialis tendon in vivo. Farron et al. [62] reported values of normalized tendon stiffness (tibialis anterior tendon) during twitch contractions to be within the range previously reported in the literature (192 MPa). Furthermore, Pearson et al. [28] compared the automated tendon-tracking method with the traditional manual method during ramped (to maximal) active and passive excursions of the patellar and medial gastrocnemius tendons, and reported no significant differences between the methods (P [ 0.05), indicating that automated tendon tracking is valid when maximal efforts are employed and also when compared with the standardized method, under different loading conditions. Thus, the method described here would prove useful for the quantification of region-specific mechanical properties in human tendons functioning in vivo, which can essentially provide valuable information relating to the etiology of patellar tendinopathy as well as the identification of potential risk factors and improvement of interventions.

To date, there is no consensus on the optimal treatment of tendinopathies. It has been suggested that the incomplete understanding of the underlying mechanisms (etiology of the condition) limits the ability to develop effective treatment strategies [63]. Indeed, this is reflected in the wide range of treatment modalities found in the literature for the management of patellar tendinopathy (i.e., non-steroidal anti-inflammatory medication; extracorporeal shock wave therapy [ESWT]; ultrasound; and various injections, including corticosteroid, platelet-rich plasma, aprotinin, and dextrose) [9]. Unfortunately, most of these have little evidence to support their use [63–68]. In contrast, conservative treatment strategies appear to be among the most favorable of interventions and form the cornerstone of patellar tendinopathy rehabilitation. The use of eccentric exercise (EE) [9, 69, 70] and heavy-slow resistance (HSR) training [71, 72], in particular, has shown very promising results with respect to the effective management of patellar tendinopathy. The following sections discuss these conservative modalities in greater detail. Table 1 also provides a comparison of the varying treatment strategies found in the literature.

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Region-Specific Tendon Properties and Patellar Tendinopathy Table 1 Comparison of patellar tendon treatment strategies Reference

Intervention

Exercise prescription

Duration

Population

Outcome

Young et al. [70]

EE on decline board

3 sets of 15 reps, twice daily

12 weeks

Elite athletes (n = 17)

Improvements in VISA and VAS scores with no differences between groups

EE on flat surface

3 sets of 15 reps, twice daily

EE on decline board

3 sets of 15 reps, twice daily

12 weeks

Recreational athletes (n = 19)

Improvements in VISA and VAS scores, 9/10 pts satisfied with tx

CE on decline board

3 sets of 15 reps, twice daily

EE (drop squats on flat surface)

3 sets of 20 reps, 59 per week

Leg extension/curl exercise

3 sets of 10 reps, 5 9 per week

EE on a decline board

3 sets of 15 reps, twice daily

EE on flat surface

3 sets of 15 reps, twice daily

Jonsson and Alfredson [74]

Cannell et al. [63]

Purdam et al. [69]

Kongsgaard et al. [71]

Kongsgaard et al. [72]

Stasinopoulos and Stasinopoulos [66]

Corticosteroid injections

No improvements in VISA or VAS scores, 9/9 pts not satisfied with tx 12 weeks

Elite athletes (n = 19)

Improvements in VAS scores with no differences between groups, 9/10 pts from EE group and 6/9 pts from leg extension/curl group returned to sport

12 weeks

Elite athletes (n = 17)

Improvements in VAS scores, 6/8 pts returned to sport

No improvements in VAS scores, only 1/9 pts returned to sport 12 weeks

Recreational athletes (n = 39)

Improvements in VISA and VAS scores but deterioration at 6-month follow-up, reduced tendon swelling and vascularization Improvements in VISA and VAS scores with maintenance at 6-month follow-up

EE on decline board

3 sets of 15 reps, twice daily

HSR training

4 sets of 6–15 reps, 3 9 per week

HSR training

4 sets of 6–15 reps, 3 9 per week

Control (healthy tendons)

4 sets of 6–15 reps, 3 9 per week

EE and stretching

3 sets of 15 reps, 39 per week

4 weeks

Elite athletes (n = 30)

Improvements in pain symptoms with EE being significantly more effective than pulsed ultrasound and transverse friction

3 sets of 15 reps, twice daily

12 weeks

Recreational athletes (n = 40)

Improvements in VISA scores at 3, 6, and 12 months of follow-up. Of 20 knees, 7 made full recovery, 8 improved but remained symptomatic at 12-month follow-up, and the remaining 5 did not benefit and underwent secondary surgery after 3–6 months

Improvements in VISA and VAS scores with maintenance at 6-month follow-up, reduced tendon swelling and vascularization and increased collagen turnover, greatest pt satisfaction at follow-up 12 weeks

Recreational athletes (n = 17)

Improvements in VISA and VAS scores, decreased tendon stiffness, changes toward normal fibril morphology (increased fibril density, decreased fibril mean area) No changes in tendon mechanical properties or fibril morphology

Pulsed ultrasound Transverse friction

Bahr et al. [68]

EE on a decline board

Surgery (wedge excision followed by rehabilitation)

Improvements in VISA scores at 3, 6, and 12 months of follow-up. Of 20 knees, 5 made full recovery, 12 had improvement but were still symptomatic, 2 were unchanged, and 1 was worse after 12 months

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S. J. Pearson, S. R. Hussain Table 1 continued Reference

Intervention

Exercise prescription

Duration

Population

Outcome

Zwerver et al. [67]

ESWT

3 ESWT tx

2 weeks

Elite athletes (n = 62)

No improvements in VISA or VAS scores at 1, 12, or 22 weeks after tx but athletes reported subjective improvement

Placebo

No improvements in VISA or VAS scores at 1, 12, or 22 weeks after tx

CE concentric exercise, EE eccentric exercise, ESWT extracorporeal shockwave therapy, HSR heavy slow resistance, pt(s) patient(s), reps repetitions, tx treatment, VAS visual analog scale, VISA Victorian Institute of Sport Assessment

5.1 Eccentric Exercise (EE) The use of EE training has been suggested to be the treatment of choice for patients suffering from patellar tendinopathy [9, 69, 70, 73]. In particular, many studies have suggested performing eccentric squats on a 25° decline board [70, 74], which more specifically targets the knee extensor mechanism (25–30 % higher patellar tendon forces) as compared with the standard eccentric squat performed on a flat surface [75, 76], and thus allows for greater tendon adaptation and improvements [70]. Concentric exercises alone, on the other hand, do not appear to have promising effects [74]. Only one randomized study to date has specifically compared the effectiveness between concentric and EE interventions, with both performed on a 25° decline board [74]. Here, benefits were only observed following the eccentric training protocol in terms of reduced pain and improved function, whereas those that performed concentric training were not satisfied and required additional treatment via injection or surgery [74]. The level of speed [77] and pain [78] in an EE rehabilitation protocol has also been of particular interest to previous researchers. There is currently no documentation concerning whether the level of speed or pain would solely have an influence on treatment effects, as no study has yet provided a direct comparison between slow and fast protocols or pain and pain-free rehabilitation protocols. However, speed and pain have previously been examined in conjunction. In particular, both slow-speed programs with pain and fast-speed programs without pain have previously shown promising results with respect to treating patellar tendinopathy [70], although there are no data indicating which modality would be most effective. While the study of Young et al. [70] did report positive effects with regards to reduced pain and improved function following slow painful and fast pain-free orientated EE training, the protocols were not matched, as one was performed on a decline board (slow painful) and the other on a flat surface (fast pain-free), making it difficult to provide a direct comparison and determine the most effective

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training modality for the management of patellar tendinopathy. Further research is clearly needed to deal with these issues. The extent of knee flexion of the eccentric squats in a rehabilitation program may also be of relevance, as previous research indicates it may perhaps have some important implications with regards to treatment effects. In particular, the posterior fascicles of the proximal tendon, which in fact correspond to the classic lesion site of patellar tendinopathy [11, 12, 16], have previously been reported to display significantly greater forces compared with anterior fascicles between 60–90° of squatting [49]. Thus, squatting beyond 60° of knee flexion could potentially expose the posterior region of the tendon to great mechanical loads and ultimately lead to subsequent injury. Therefore, it has been suggested that squatting should be limited to no greater than 60–70° of knee flexion [49, 70, 79], due to the excessive forces on the patellofemoral joint, patellar tendon, and the meniscus [80]. On the other hand, some studies also encourage full-depth squats to 90° of knee flexion [69, 74], although this should be interpreted with caution, as full-depth squats may be particularly difficult to perform in the clinical setting due to excess pain. Additionally, no data currently exist concerning the optimal program design variables (i.e., intensity, volume, frequency) for an EE rehabilitation program that would promote the greatest benefits for patellar tendinopathy patients. The majority of previous investigations have utilized a volume of three sets of 15 repetitions on a 25° decline board twice a day to improve tendon pain and function [70, 74, 80–82], although the total number of sessions have varied considerably between studies. Also, exercise intensities have only been previously assigned through manipulations of speed or the amount of extra weight added on to the individual, typically progressed by either increasing load [78] or by increasing speed and then load [70]. However, once again, these contrasting prescriptions have not previously been directly compared and thus it would seem very difficult to provide ideal program design variables from the existing literature.

Region-Specific Tendon Properties and Patellar Tendinopathy

5.2 Heavy-Slow Resistance Exercise (HSR) The use of isotonic HSR training is not as well studied as EE training but has also shown very promising results [71, 72]. Kongsgaard et al. [72] examined the effects of a 12-week HSR training program in a cohort of elite athletes with patellar tendinopathy. Results showed significant improvements in symptoms/function and maximal tendon pain during activity. In addition, tendon stiffness was found to decrease (mean ± SD 3,185 ± 187 to 2,701 ± 201 N
mm-1, P \ 0.05) but fibril density increased (mean 70 %) and fibril mean area decreased (mean 26 %), showing a change towards normal fibril morphology. Thus, HSR training may also be particularly useful with regards to alleviating symptoms for effective management of the condition. However, it is currently unclear whether HSR would be any more effective than EE training in the management of patellar tendinopathy since there are few studies available that directly compare these modalities. Interestingly, though, the one study of Kongsgaard et al. [71] did conduct a direct comparison between the effects of corticosteroid injections, EE training, and HSR training in a randomized, single-blinded fashion. All treatments were found to improve Victorian Institute of Sport Assessment (VISA) and visual analog scale (VAS) scores, but this was only maintained in the EE and HSR groups at the 6-month follow-up, indicating that corticosteroid injections may only provide short-term clinical benefits. Tendon swelling (mean 13 and 12 %) and vascularization (mean 52 and 45 %) were also decreased significantly following corticosteroid injections and HSR training, respectively. In addition, tendon mechanical properties remained unchanged following all treatments; however, HSR yielded a significantly elevated collagen turnover. Moreover, at the 6-month follow-up, treatment satisfaction differed between groups, with the HSR group being the most satisfied. Based on these considerations, it appears that HSR training can have short- and long-term clinical effects with respect to pathology improvement and subsequent tendon adaptation, and may even be somewhat more effective than EE training in patellar tendinopathy management. This notion is also supported by Malliaras et al. [83], who conducted a systematic review and reported HSR loading to have an equivalent or higher level of evidence in terms of clinical outcomes compared with EE training. In particular, the authors found HSR loading in the patellar tendon to be associated with reduced Doppler area and anteroposterior diameter, as well as greater collagen turnover, which is not found following EE loading. However, since there is currently a paucity of research directly comparing HSR and EE training, it would be premature to determine which is the most favorable conservative treatment strategy.

Furthermore, no evidence currently exists in terms of the optimal program design variables of an HSR rehabilitation program that would elicit the most favorable effects. The few studies available on patellar tendinopathy rehabilitation have utilized a program consisting of four sets of 6–15 repetitions, performed 3 times per week for successful management of the condition [71, 72]. However, further studies that directly compare varying exercise prescriptive variables are required. 5.3 Limitations It is noteworthy that there are limitations to the majority of previous rehabilitation investigations in that they have merely estimated tendon function through VISA and VAS scores [69, 70, 74], and have not directly determined the functionality of the tendon via an assessment of the structural and mechanical properties. To the authors’ knowledge, only two studies to date have directly determined the effects of a rehabilitation program on the tendon mechanical properties [71, 72], one of which reported a decrease in tendon stiffness [71], whereas the other reported no change [72] in response to HSR training protocols. However, both studies examined the tendon structure as a whole and as such have not provided any insight in terms of how each discrete region of the tendon alters with rehabilitation, which is very important considering that patellar tendinopathy is a region-specific condition. This is indeed a problem if the true effectiveness of rehabilitation programs on the management of patellar tendinopathy is to be determined. Thus, it is stressed here that it would seem beneficial for future research to quantify the region-specific structural and mechanical properties of the tendon in rehabilitation studies to determine and/or develop the most favorable treatment strategy for patellar tendinopathy.

6 Conclusions Patellar tendinopathy is a common musculoskeletal disorder affecting a wide range of recreational and elite athletes, with those that participate in jumping events being the most susceptible. The underlying pathophysiology is, to date, still poorly understood, although it may perhaps relate to intra-tendinous variations in loading patterns and mechanical properties between the different regions of the tendon. However, research concerning the in vivo regionspecific tendon properties is very scarce due to the lack of validated techniques that can determine such properties, but more recently a technique has been established. It has also been validated [28] and utilized by many studies for the determination of region-specific mechanical properties

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in vivo [29, 30], ultimately highlighting its efficacy to be used by future patellar tendinopathy studies. The structural tendon changes with patellar tendinopathy are most frequently associated with the proximal posterior region of the tendon, although the quantification of each discrete region of the tendon in terms of length and CSA is yet to be documented. However, based on previous case–control studies, tendinopathy appears to result in an increased tendon CSA concomitant with decreased stiffness and Young’s modulus. These changes are most likely due to alterations in the tendon tissue arrangement and composition, which in turn may adversely affect muscle function and injury risk. Moreover, data on region specific mechanical properties of the patellar tendon have shown conflicting results, in that some studies support the tensileoverload theory whereby the posterior region of the tendon is subjected to greater tensile strain than the anterior region, thus leading to potential posterior tendon overuse with repetitive loading, and others support the stress shielded theory, whereby the posterior region of the patellar tendon does not exhibit a higher magnitude of tensile strain than the anterior region in the functional flexion range and is, consequently, stress shielded. Additionally, research on differences in biochemical properties between different tendon regions suggest that variations exist with respect to HP and LP cross-link concentration; however, this dissimilarity in biochemical properties is not associated with tendon mechanical properties (strength). Thus, other factors may contribute to tensile function and strength. Collectively, there appears to be evidence to support the notion that differences exist with regards to structural, mechanical, and biochemical properties between the discrete regions of the tendon. However, the extent to which these region-specific differences contribute to patellar tendinopathy is not well understood and warrants further investigation. In terms of conservative treatment strategies, a wide range have been utilized for the management of patellar tendinopathy, but the use of EE and HSR training, in particular, appear to be most promising. However, the optimal exercise prescriptive variables of these modalities are still to be determined. Moreover, the majority of previous rehabilitation investigations aimed at treating patellar tendinopathy have merely assessed tendon function through VISA and VAS scores, which does not provide a direct measure of the functionality of the tendon or any information in terms of regional changes. This could potentially present a problem in assessing the efficacy of rehabilitation programs and ultimately determining the most effective treatment strategy. Therefore, it may be most useful to directly assess the region-specific tendon properties in future patellar tendinopathy rehabilitation studies for the improvement of treatment interventions.

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A better understanding of region-specific tendon properties will provide invaluable information relating to the etiology of patellar tendinopathy as well as the identification of potential risk factors and most effective treatment strategies, which in theory could improve clinical knowledge. For instance, if a specific region of the tendon is found to be subjected to the greatest magnitude of tensile strain during contractile activity, it would lend some perspective in relation to the etiology, and so, any activity that exposes this region of the tendon to the largest forces could be considered a potential risk factor. Preventive public health policies and/or targeted rehabilitation strategies could therefore be designed to specifically prevent and/or alleviate symptoms in the affected region of the tendon for effective management of the condition, ultimately assisting in the development of the most effective treatment strategy. Moreover, since patellar tendinopathy is region specific, the determination of region-specific tendon properties would provide useful normative data that can be used by clinicians for improved diagnosis and patient advice. Acknowledgments No funding was provided in the preparation of this review, and the authors have no conflicts of interest that are directly relevant to the contents of the review.

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