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 Biomechanics of the Knee Extensor Mechanism and Its Relationship to Patella Tendinopathy: A Review

Michael Dan,1,2 William Parr,1 David Broe,1,2 Mervyn Cross,3 William R. Walsh1,2

1Surgical and Orthopaedic Research Laboratory, Prince of Wales Clinical School University of New South Wales, Sydney 2052, Australia, 2Prince of Wales Hospital, Barker St, Randwick, New South Wales 2031, Australia, 3The Stadium Sports Medicine Clinic, Sydney 2012, Australia Received 29 May 2018; accepted 26 July 2018 Published online 3 August 2018 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/jor.24120

ABSTRACT: The term jumpers knee for patella tendinitis, as coined by Dr. Martin Blazina, is now commonly referred to as tendinopathy. He believed it was associated with patella alta. Since then multiple studies have failed to reliably show an association between patella tendinopathy and associated intrinsic risk factors. There is, unfortunately, a well-established doctrine that the extensor mechanism is simply a pulley. The goal of the review is to examine the biomechanics of the extensor mechanism and apply this to studies investigating intrinsic risk factors for patella tendinopathy. A better understanding of the biomechanics of the extensor mechanism may stimulate the discovery of intrinsic risk factors for developing patella tendinopathy, and subsequent surgical options to address them. Clinical significance: The aim of this review is to direct future research into biomechanical risk factors for developing patella tendinopathy and subsequently, possible treatments. ß 2018 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 36:3105–3112, 2018.

Keywords: patellar tendinopathy; jumper’s knee

Patella tendinopathy is an overuse condition largely as reported by Amiel and co-workers in 1983. When affecting high level athletes involved in jumping compared with the knee ligaments from a histological sports.1 The relatively poor clinical outcomes are and biochemical view the connective tissue connecting reflected by the fact there is a multitude of treatment the patella bone to the tibia more closely resembles options for patella tendinopathy, this intuitively means tendon (Achilles) more so than ligament. Microscopi- that one cannot be vastly superior to another nor can cally it is more hypocellular, containing longer spindle- one be truly effective.2 The aim of this review is to shaped fibrocytes which are more regularly arranged correlate the extensor mechanism biomechanics with than ligaments (larger and rounder cells less regularly patella tendinopathy in the hope of directing future arranged). Biochemically the patella tendon had a research and treatments to improve clinical outcomes. higher collagen content, but a smaller percentage of type III collagen (5% for tendons vs. 10–12% for ANATOMY ligaments), less DNA, and glycosaminoglycan content, and a higher number of hydroxylysinonorleucine cross- The extensor mechanism is responsible for extending links relative to dihydroxylysinonorleucine (reverse for the tibiofemoral joint. The term refers to the common ligaments).4 Therefore we will refer to it as the patella linkage of the four converging quadriceps muscles into tendon. the quadriceps tendon attaching proximally to the The type I collagen forms the fascicles which are patella bone, continued distally by the patella liga- the subunits of tendon hierarchy. There are anatomi- ment or tendon to the tibial tuberosity.3 The patella is cal differences within the human patella tendon. The a sesamoid bone and articulates with the trochlea of posterior fascicles, when compared to the anterior the femur, forming the patellofemoral joint- capable of fascicles, have been shown to be smaller in diameter, 6 degrees of movement. shorter and have higher concentration of cross linked Confusion exists concerning nomenclature of the hydroxylysylpyridinoline5 which reflects mature colla- Patella tendon or patella ligament. Both have been gen crosslinks and a robust mechanical construct. used interchangeably as tendon and ligaments are thick closely packed collagenous bundles orientated parallel to the long axis of the structure.4 Macroscop- PATELLA TENDINOPATHY ically, it can be argued to fit either definition. It Patella tendinopathy continues to be an area of connects the patella (bone) to the tibia (bone) which is interest (Figure 1) for nearly 5 decades reflecting the the definition of a ligament (bone to bone connection). search for better understanding of the pathology and However, functionally the patella tendon connects the need for improved clinical solutions. quadriceps muscle to the tibia bone, with the patella as Patella tendinopathy is an overuse condition affect- a sesamoid bone within it. This is also the macroscopic ing mostly athletes. It was initially described by Dr. definition of a tendon, which connects muscle to bone. Martin Blazina in 1973 is his description of jumper’s From a histological and biochemical view it is a tendon knee.6 While jumper’s knee includes pain at the quadriceps insertion (25% of cases), distal pole of patella (65%), and the tibial tubercle insertion (10%),7 Grant sponsor: The Australian Government. Correspondence to: Michael Dan (T: þ61428082964; F: 02 9382 the enthesiopathy of the patella tendon at the distal 2660; E-mail: [email protected]) pole of the patella is the definition of patella tendinop- # 2018 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. athy (see in Figure 2).

1 JOURNAL OF ORTHOPAEDIC RESEARCH DECEMBER 2018 3105

 3106 DAN ET AL.

Figure 1. Time line of Patella tendinopathy from first description to current trends in clinical practice.

Originally described as tendinitis, histologically it the fibrocartilage to the mineralized fibrocartilage junc- lacks inflammation.8,9 The tendinopathy is characterized tion. Loss of alignment occurs as within the fibers as by microtearing of the tendon and local mucoid degener- mucoid ground substance separates the normally paral- ation and fibrinoid necrosis, with loss of transition from lel collagen bundles. There is increased cellularity due to the proliferation of fibroblasts and neovascularisation.10 There is a lack of inflammatory cells and there is no increase in prostaglandin expression, signifying an ab- sence of inflammation.10,11 Clinically patella tendinopathy is characterized by symptoms of specific anterior knee pain and tenderness localized at the distal pole of the patella.6 The diagnosis is primarily clinical but is supported by imaging findings on ultrasound show thickening of the tendon and a characteristic heterogeneous echogenicity.12 On MRI, blurry ligamentous margins and increased signal intensity within the patella tendon on both short and long TE sequences. X rays are done to exclude other pathologies such as Osgood-Schlatter13,14 and Sinding- Larsen-Johansson disease,15 but do not show specific signs to patella tendinopathy.16 There are two classification systems to grade sever- ity. Historically, Blazina divided it into clinical phases 1 through 3. This gives a good qualitative description of the clinical progression of the disease. Phase 1 is pain post exercise, phase 2 is characterized by pain at the beginning and end of activity but is absent post “warm up,” phase 3 is pain during and after activity.6 Phase 4, later added by Roel, represents complete tendon rupture.10 To better quantify severity and response to treat- ment, the Victorian Institute of Sport Assessment (VISA) scale is used.17 Designed 1998 the VISA scale consists of a series of eight questions with a total score out of 100. Examples of mean scores, with associated standard deviation include; 95 þ 8 for asymptomatic individuals, 55 þ 12 for those with the disease partici- pating in sport, 22 þ 17 for those requiring surgery Figure 2. Affect of flexion on the Patella tendon to Quadriceps with expected 6 and 12 month improvements of tendon force ratio. Graph shows the overall trend. For the first þ þ 17 part of flexion the force in the patella tendon is greater than the 49 15 and 75 17 points correspondingly. force in the Quadriceps tendon. The reverse is true as the knee Once affected by patella tendinopathy the prognosis is continues to flex. The Anatomical drawings depict this relation- ship demonstrating the distal pole of the patella articulating with poor; Kettunen followed 36 athletes over a 15 year period. the Femur in extension (a) and in flexion the proximal articular Of the 20 with patella tendinopathy, 53% were forced to surface articulates with femur (b). F ¼ Femur, FQT ¼ force in ¼ ¼ retire from sport due to the condition. This is in compari- Quadriceps Tendon, FPT Force in Patella Tendon, P Patella, 18 T ¼ Tibia, ¼ location of patella tendinopathy. son to 7% of control athletes retiring due to injury.

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 BIOMECHANICS OF PATELLA TENDINOPATHY: REVIEW 3107

Non operative management is the main form of increasing it’s relative lever arm (Figure 2b). While the treatment; this includes physiotherapy, load manage- magnitudeofstressineachtendoncanchangeaccording ment, and injectables. Roughly 10% of patients require to the applied quadriceps force, the ratio of the stress surgery.19 This includes patients in stage 3 and 4. between the two tendons is constant for a given flexion Surgery can be performed in an open fashion or angle. Whilst the reported ratios differ between papers, arthroscopically. It consists of removal of the patholog- the principle has been confirmed in a number of further ical portion of the tendon (labeled in Figure 1), with or biomechanical cadaver and Finite Element Analyses.39–41 without drilling of the patella to stimulate new blood There are location dependent morphological and flow in an attempt to promote healing.2,20–27 biomechanical variations within ligaments and tendon. Case series report good results for surgery, gener- The ACL is the most studied ligament, it was the first ally in excess of 80% regardless of technique utilized, to demonstrate location of orientation dependent prop- however a systematic review found that the reported erties. The ACL is known to experience greater loads level of successful outcomes was inversely proportional to failure when loaded in the anatomical orientation to the level of evidence.28 Bahr and co-workers ques- maintaining its natural insertion angles compared tioned the clinical effectiveness of surgery in 2006 with aligning to the axis of the tibia.42,43 The aim of with high level clinical evidence- with a randomized the proceeding paragraphs will be to explore the control trial showing no difference in outcomes be- biomechanical strain properties of the patella tendon tween surgery and physiotherapy.29 and correlate these with suggested etiologies for Given the poor clinical outcomes combined with a patella tendinopathy. multitude of treatment options, this review article A cadaver study performed by Almekinders44 found aims to outline how differences in the extensor mecha- the tensile strain decreased in the posterior proximal nism biomechanics are linked to proposed risk factors part of the patella tendon but increased in the anterior for patella tendinopathy in the hope of guiding future proximal portion of the tendon throughout flexion. research to advance treatment. Low quadriceps loads of 13-58N were applied. Alme- kinders et al concluded that stress shielding may be EXTENSOR MECHANISM BIOMECHANICS the pathogenesis for patella tendinopathy. However The Latin translation of trochlea(e) is pulley. The the patella tendon force was not reported and the patella was long viewed a pulley whose role was to stress was not actually calculated. In comparison the change the direction of the quadriceps force, but not forthcoming biomechanical studies support the hy- its magnitude,30,31 and an underestimation of its pothesized pathogenesis of repetitive microtrauma function can still be found today.32–34 caused by overload. The patella cartilage, the thickest in the body,35 The morphological differences explained by Hansen makes the extensor mechanism a near frictionless from healthy patella tendons harvested as part of ACL system reducing coefficient of friction by having articu- reconstruction surgery translated to biomechanical lar cartilage on articular cartilage (0.005–0.02) versus differences with the anterior fibrils having a higher tendon on cartilage.36 Kaufer’s biomechanical cadaver tensile load to failure and were stiffer than the shorter study was an improvement in demonstrating the and smaller posterior fibrils which experienced greater biomechanical effect of the patella thickness in in- strain.5 Basso et al45 applied higher loads of 1,000 N in creasing the moment arm of the extensor mechanism, their cadaver model than Almekinders44 and found a thereby increasing the efficiency of the quadriceps. significant difference between strain in the anterior Patellectomy results in an increase of the force and posterior bundles, with strain being higher in the required from the quadriceps to achieve full extension posterior fibers and increasing between 60 and 90 compared to the normal knee by 130%.37 degrees of flexion. The posterior fibers of the patella Huberti38 was the first to recognize the extensor tendon are shorter than the anterior fibers, this mechanism was not a true pulley. In their cadaver anatomical relationship is in keeping with the poste- model, they were able to demonstrate that the force rior fibers experiencing a greater strain for a given between the patella and quadriceps tendon is not applied force due to the relative difference in initial equal, and the ratio between the two changes with length compared to the anterior fibers. knee flexion. This ratio is greater than 1 from 0 to 45 PPTA is Patella-Patella Tendon Angle (Lavagnino degrees of flexion and then the patella and quadriceps et al),46 it is the angle formed between the patella tendon tendon becomes less than one for degrees of flexion and patella angle. This study built an FEA model and greater than 45 degrees. As seen in Figure 2. validated the model using cadaver tissue. A jig was They stipulated that this was the result of changing utilized which removed the quadriceps tendon and the the contact area within the patella. When viewed as a femur to isolate the amount and location of maximum lever, the quadriceps tendon acts with a longer lever arm strain and stress within the patella tendon (see Figure 3). in extension giving it a mechanical advantage The location was at the superior and posterior part of (Figure 2a), where as in flexion the patella contact area the patella tendon- corresponding to the location of with the femur moves to the proximal pole of the patella, patella tendinopathy. The stress was found to be tensile giving the patella tendon a mechanical advantage by rather than compressive- biomechanically eliminating a

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 3108 DAN ET AL.

tendon (see Figure 4). The individual contribution of a shorter tendon, while keeping these other parameters constant, has not been explored50 but is thought to undergo higher amounts of strain for a applied Force, with greater stress within a smaller tendon.45 Therefore it can be considered that the main determinants of the patella tendon force are the angle between the tendon and the patella axis and the location of the femoral contact point on the patella. The effect of the contact point predominates over the angle formed.48 This relationship can be simplified through the equilibrium of moments. When the patella is viewed as a lever- for there to be an equilibrium of moments, the torques on either end of the patella have to be equal. Figure 5 demonstrates this relationship. Torque is equal to force multiplied by the perpendicular distance from the point of rotation (LAQT and LAPT). Applied to a lever the torque is equal to the lever arm multiplied by the perpendicular force. When the lever arms formed by the distance from the articulation point (fulcrum) to the insertion point of the respective tendon are equal and the angle between the quadri- ceps/patella tendon and the perpendicular component of the force are equal, the system is in equilirum. Figure 5 demonstrates that as the patella moves Figure 3. Tendon orientation and changes to patella tendon distally the lever point will change and the lever arm strain. Reproduction of jig used by Lavagnino et al to measure for the patella tendon side becomes longer. Keeping strain changes within the patella tendon as the angle between the patella tendon and patella bone (PPTA) ¼ u changed. As the the joint reaction force the same, and changing the PPTA decreased from 162 to 145˚ (corresponding to 0–60˚ of knee lever arm ratio from 2:2 to 1:3, the torque required flexion), the maximum point strain and the mean localized strain from the patella tendon is third the value required increased significantly within the posterior superior aspect of the tendon- a biomechanical explanation for the location of patella from the quadriceps. tendinopathy. The effect is also demonstrated of changing the tilt of the patella bone relative to the patella tendon. As compressive etiology to patella tendinopathy. As the the tilt of the patella bone aligns with the direction of PPTA decreased from 162˚ to 145˚ (corresponding to the patella tendon force, the force required within the 0–60˚ of knee flexion), the maximum point strain and patella tendon to achieve the same torque increases. the mean localized strain increased significantly within Torque is equal to the cosine of the angle u formed the posterior superior aspect of the tendon. The applied between the tendon and the moment force multiplied Force was up to 4250 N, again significantly higher than by the force in the patella tendon, for a constant that applied by Almekinders,44 like Basso45 reflecting distance from rotation (see Figure 5). As that angle, u the load and range of motion occurring during jumping approaches zero, the cosine u becomes 1, meaning the and landing.47 force required in the patella tendon is the same as Van Eijden came up with a series of nine non-linear the moment, as this angle approaches 90 degrees the equations which could be used to describe: (1) the force required in the patella tendon to produce the position of patellar ligament, patella, and quadriceps same torque approaches infinity, cosine 30 ¼ 0.87, tendon; (2) the contact point of the patellofemoral cosine 60 ¼ 0.5 cosine 75 ¼ 0.25, cosine 85 ¼ 0.09. How- joint; and (3) the ratio between the patella tendon ever as described earlier- the contribution of the angle force: quadriceps force and the quadriceps force: is complicated by the inherent fibril anatomy and patellofemoral joint contact force ratio for a given knee morphology, this alters how tendon orientation will and flexion angle.48,49 dictate the strain pattern, and the required load to The position of the patella changes between relaxa- failure of a applied tensile force. tion and contraction. Determing factors include it’s individual and the femur’s morphology, the position of RISK FACTORS thetibialtuberclerelativetothefemur,thelengthand Risk factors can be divided into extrinsic and intrin- position of the patella tendon and the quadriceps tendon. sic. Extrinsic account for the nature of the stimuli The length of the patella tendon affects the patella outside the athlete and intrinsic are somatic to the tendon force, as it changes the patella contact position athlete/patient. Soslowsky has documented the contri- and the angle between the patella axis and the patella bution of each to supraspinatus tendinopathy in the

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 BIOMECHANICS OF PATELLA TENDINOPATHY: REVIEW 3109

Figure 4. Patella positioning as patella tendon length (LPT) changes. Length in (a, b, and c). As a consequence of decreased LPT the proximal part of the patella will articulate with the femur, giving a long lever arm to the patella tendon and decreasing the force through it to achieve the same torque, even with an increased angle between the patella and patella tendon. QT ¼ Quadriceps tendon, LPT ¼ Length of Patella Tendon, LAQT ¼ Lever arm Quadriceps tendon, LAPT ¼ Lever arm Patella tendon. rat, regardless of the intrinsic risk factors without prevalence of greater than 50% in basketball and the appropriate extrinsic risk factors—tendinopathy volleyball players, between 20 and 30% for team will not develop.51,52 While extrinsic risk factors have handball, soccer, and ice hockey, where as there was a been proven for patella tendinopathy, identifying 0% prevalence in cyclists.1 morphological intrinsic risk factors have proven elu- Further supporting the load aetiology is increased sive and we will explore the reasons for this. training load and harder training surfaces are gener- ally accepted as being correlated with development of Extrinsic jumper’s knee/patella tendinopathy,53,54 accepting In keeping with the pathogenesis of repetitive overload there are some papers which disagree.55 causing micro trauma to the patella tendon, external stimuli to increase patella tendon load have been Intrinsic shown to increase the incidence of patella tendinop- Blazina only ever made qualitative observations in his athy. Different sports have a higher incidence of original case series. He noted the athlete was “usually patella tendinopathy, namely those requiring a lot of tall” and had abnormalities of the extensor mechanism- jumping. Lian et al in a cross sectional study found an including- wasting hyper mobility, genu recurvatum,

Figure 5. Patella as a Lever. Torques on either side must balance to be equilibrium. Torque ¼ LA x F?. (a) LAQT ¼ LAPT.F?QT ¼ F?PT, u is the same, therefore FQT¼FPT. (b) Keeping u equal, Increasing the LAPT will decrease the required F?PT, and decrease the FPT. Consequently the LAQT will decrease and the required F?QT and FQT will increase. (c) Keeping the lever arm constant but increasing the u between the patella tendon and F?PT will increase the FPT required for equilibrium. Key- LAQT ¼ Lever arm Quadriceps tendon, LAPT ¼ Lever arm Patella tendon, FQT ¼ Force Quadriceps tendon, FPT ¼ Force Patella Tendon, F?PT ¼ Force perpendicular to the LAPT, F?QT ¼ Force perpendicular to the LAQT. u ¼ angle between F? and tendon. Magnitudes are visually reflected by changes the size, capitalization and type of font.

1 JOURNAL OF ORTHOPAEDIC RESEARCH NOVEMBER 2018

 3110 DAN ET AL. and valgus, patella alta in “certain cases” but never compressive etiology. They found no statistical differ- statistically analyzed or quantified this statement. On ence in the shape of the patella, which was previously radiographic examination he noted an elongated infe- observed by other authors but never quantified (i.e., rior pole of the patella, patella alta, and chondromala- elongated distal pole) or the angle formed between the cia “has been seen in some cases” and noted differences patella and patella tendon between groups. This is in the insertion of the patella tendon but “could not radiographic evidence that reaffirms Lavagnino’s FEA draw any specific conclusions as to the contribution of and cadaver’s results that patella tendinopathy is not this particular method in the study of ‘jumper’s knee’ .” due to a compressive etiology.24 The first attempts to quantify a difference in When reviewing factors outside the knee- a system- incidence of abnormal patella morphology associated atic review concluded that there was insufficient with patella tendinopathy was by Roel. Roel stated evidence to attribute age, body habitus- height, there was elongation of the inferior pole of the patella weight/BMI/skin folds to patella tendinopathy, how- 1 out of 22 patients in the conservative group versus 4 ever it was associated with limb length discrepancies of 10 in the group requiring surgery. Three of the 10 and loss of the medial arch of the foot.55 in the surgical group had a “high” patella (patella Witvrouw et al58 performed the only prospective alta). No quantification or method of patella height study done to evaluate the development of patella measurement of this was given though.10 Ferrati noted tendinopathy with time in an athletic population. At distal pole elongation in 9 of 125 patients.7 the onset of the study different parameters were Verheyden noted that the four patients who had a measured. These included body proportions, anatomi- “poor” result (author defined scoring system) out of the cal morphology, muscle flexibility, and strength. Fol- 31 treated surgically, all had evidence of patellofe- lowed over a 2 year period 19 of the 138 athletes moral maltracking. This being patella tilt and sublux- developed patella tendinopathy. Differences in ham- ation, and suggested this should be addressed at the string and quadriceps flexibility were the only statisti- time of surgery. However they did not quantify or cal differences.58 comment on any patellofemoral abnormalities, or lack of, in those who had a successful operation.56 CONCLUSION WHAT IS UNKNOWN AND WHAT Ferretti performed proximal realignment (VMO DO WE NEED TO KNOW MOVING FORWARD advancement and lateral release) in those with concur- There is a multitude of treatments for patella tendinop- rent patella femoral malalignment. They never quali- athy, this intuitively means that one cannot be vastly tatively described what malalignment existed or superior to another nor can one be truly effective. quantified this further in their original description.7 Many believe the future to tendon injuries and Ferretti however changed his viewed with time. In a tendinopathies lie in cell based therapy,59,60 however case control series, statistical analysis of 26 patients attempts to repair tissue without altering the intrinsic with jumper’s knee while extensor mechanism abnor- biomechanical reason for failure can only lead to the malities were noted as listed above the incidence was return of symptoms. not increased in comparison with 96 athletes who did If we consider the aetiology of patella tendinopathy not suffer from jumper’s knee, leading him to conclude to be repetitive overload causing microtears. Extrin- that intrinsic risk factors were not associated with the sically as the external environment changes, most development of patella tendinopathy.54 commonly via higher training loads in jumping associ- Tyler and co-workers57 examined patella tilt in the ated sports, the incidence of patella tendinopathy sagittal plane with reference to the femoral axis in increases. However, while all athletes/patients are radiographs. Tyler and co-workers noted that there was exposed to the same external stimulus, not all athletes differences in the degree of flexion of the lateral radio- develop patella tendinopathy. As identified by Soslow- graph in the normal populations. The patella tilt was sky in the pathogenesis of supraspinatus tendinopathy correlated with knee flexion- increasing with increased in the rat,51,52 there too must be some intrinsic risk knee flexion. Tendinopathy patients had a reduced patella factors which increase the susceptibility of certain tilt relative to normal subjects. The authors did not individuals to develop patella tendinopathy. explain why this would be an associated risk factor. Unfortunately, morphological intrinsic risk factors Assuming there was no difference between the mean continue to be cited today2 as a result of observations angle of the knee X-rays in the normal versus the patella made in the 1970s which were never statistically quanti- tendinopathy patients (not stated in the paper), we fied and in the case of Ferretti54 later self-disproved. hypothesize, according to Van Eijden,48 that a reduced Attempts to identify intrinsic risk factors for patella patella tilt angle would be the result of a patella which tendinopathy have largely focused on applying what is articulates with its distal pole for longer, resulting in an known from patellofemoral dislocation to patella ten- increased patella tendon to quadriceps tendon force ratio. dinopathy. Patella height is largely referenced with This would predispose the patella tendinopathy patients respect to the tibia, this has an indirect affect, maybe to higher stress through their patella tendon. variable (not investigated) on what part of the patella A case control MRI paper dynamically looked at articulates with the femur throughout flexion and an knees from 0 to 100 degrees of flexion; examining for a inconsistent effect on patella tendon biomechanics.

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 BIOMECHANICS OF PATELLA TENDINOPATHY: REVIEW 3111

Patella tilt, Q angle, tibial tubercle- trochlea groove interpretation of data; (2) drafting the paper or revis- distance may all affect how the patella tendon fibers ing it critically; and (3) approval of the submitted and are orientated for an applied quadriceps force. This final versions. All authors have read and approved the could subsequently the strain with force within the final submitted manuscript. patella tendon. However taken in isolation these factors have not been associated with patella tendinopathy. ACKNOWLEDGMENTS As identified by Huberti the patella should be viewed Dr. Michael Dan would like to acknowledge the financial as a lever with a fulcrum that moves pending the support he receives with the Research Training Program degree of knee flexion, being mechanically advanta- stipend scholarship from the Australian government to do geous for the quadriceps tendon in extension and the his PhD. patella tendon in flexion.38 Attempts to identify intrin- sic morphological risk factors should focus on this REFERENCES relationship moving forward. It would be of note if the 1. Lian OB, Engebretsen L, Bahr R. 2005. Prevalence of fulcrum has a mechanically disadvantageous position jumper’s knee among elite athletes from different sports: a for the patella tendon in those subjects with patella cross-sectional study. Am J Sports Med 33:561–567. tendinopathy relative to those athletes without the 2. Figueroa D, Figueroa F, Calvo R. 2016. Patellar tendinopathy: diagnosis and treatment. 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Force ratios patellar tendinitis with use of a new radiographic measure- in the quadriceps tendon and ligamentum patellae. J Orthop ment. Am J Sports Med 30:396–401. Res 2:49–54. 58. Witvrouw E, Bellemans J, Lysens R, et al. 2001. Intrinsic 39. Buff HU, Jones LC, Hungerford DS. 1988. Experimental risk factors for the development of patellar tendinitis in an determination of forces transmitted through the patello- athletic population. A two-year prospective study. Am J femoral joint. J Biomech 21:17–23. Sports Med 29:190–195. 40. Heegaard J, Leyvraz PF, Curnier A, et al. 1995. The 59. Gaspar D, Spanoudes K, Holladay C, et al. 2015. Progress in biomechanics of the human patella during passive knee cell-based therapies for tendon repair. Adv Drug Deliv Rev flexion. J Biomech 28:1265–1279. 84:240–256. 41. Ali AA, Shalhoub SS, Cyr AJ, et al. 2016. Validation of predicted 60. Clarke AW, Alyas F, Morris T, et al. 2010. Skin-derived patellofemoral mechanics in a finite element model of the tenocyte-like cells for the treatment of patellar tendinop- healthy and cruciate-deficient knee. J Biomech 49:302–309. athy. T Am J Sports Med 39:614–623.

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Surgery for patellar tendinopathy (jumper’s knee) (Review)

Dan M, Phillips A, Johnston RV, Harris IA

Dan M, Phillips A, Johnston RV, Harris IA. Surgery for patellar tendinopathy (jumper’s knee). Cochrane Database of Systematic Reviews 2019, Issue 9. Art. No.: CD013034. DOI: 10.1002/14651858.CD013034.pub2.

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Surgery for patellar tendinopathy (jumper’s knee) (Review) Copyright © 2019 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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T A B L E O F C O N T E N T S HEADER...... 1 ABSTRACT...... 1 PLAIN LANGUAGE SUMMARY...... 2 SUMMARY OF FINDINGS...... 4 BACKGROUND...... 8 OBJECTIVES...... 8 METHODS...... 9 RESULTS...... 12 Figure 1...... 13 Figure 2...... 15 Figure 3...... 16 DISCUSSION...... 18 AUTHORS' CONCLUSIONS...... 19 ACKNOWLEDGEMENTS...... 20 REFERENCES...... 21 CHARACTERISTICS OF STUDIES...... 23 DATA AND ANALYSES...... 29 Analysis 1.1. Comparison 1 Open surgical excision vs eccentric exercises, Outcome 1 Knee Pain- standing jump...... 29 Analysis 1.2. Comparison 1 Open surgical excision vs eccentric exercises, Outcome 2 Function (VISA) 0 to 100, 100 best...... 30 Analysis 1.3. Comparison 1 Open surgical excision vs eccentric exercises, Outcome 3 Global success - Proportion with no 30 symptoms at 12 months...... Analysis 1.4. Comparison 1 Open surgical excision vs eccentric exercises, Outcome 4 Global assessment of success...... 30 Analysis 1.5. Comparison 1 Open surgical excision vs eccentric exercises, Outcome 5 Return to sport...... 30 Analysis 2.1. Comparison 2 Surgery (arthroscopic) vs sclerosing injection, Outcome 1 Knee pain- functional VAS...... 31 Analysis 2.2. Comparison 2 Surgery (arthroscopic) vs sclerosing injection, Outcome 2 Global outcome of success- Satisfaction 31 VAS...... Analysis 2.3. Comparison 2 Surgery (arthroscopic) vs sclerosing injection, Outcome 3 Withdrawal rate...... 31 APPENDICES...... 32 HISTORY...... 34 CONTRIBUTIONS OF AUTHORS...... 34 DECLARATIONS OF INTEREST...... 34 SOURCES OF SUPPORT...... 35 DIFFERENCES BETWEEN PROTOCOL AND REVIEW...... 35 INDEX TERMS...... 35

Surgery for patellar tendinopathy (jumper’s knee) (Review) i Copyright © 2019 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

 Cochrane Trusted evidence. Informed decisions. Library Better health. Cochrane Database of Systematic Reviews

[Intervention Review] Surgery for patellar tendinopathy (jumper’s knee)

Michael Dan1, Alfred Phillips2, Renea V Johnston3, Ian A Harris4

1University of New South Wales, Liverpool, Australia. 2Hunter New England Health District, University of New South Wales, Liverool, Australia. 3Monash Department of Clinical Epidemiology, Cabrini Institute and Department of Epidemiology and Preventive Medicine, School of Public Health and Preventive Medicine, Monash University, Melbourne, Australia. 4Ingham Institute for Applied Medical Research, South Western Sydney Clinical School, University of New South Wales, Liverpool, Australia

Contact address: Michael Dan, University of New South Wales, Liverpool, Australia. [email protected].

Editorial group: Cochrane Musculoskeletal Group Publication status and date: New, published in Issue 9, 2019.

Citation: Dan M, Phillips A, Johnston RV, Harris IA. Surgery for patellar tendinopathy (jumper’s knee). Cochrane Database of Systematic Reviews 2019, Issue 9. Art. No.: CD013034. DOI: 10.1002/14651858.CD013034.pub2.

Copyright © 2019 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

A B S T R A C T

Background Patellar tendinopathy is an overuse condition that commonly affects athletes. Surgery is usually offered if medical and physical therapies fail to treat it effectively. There is variation in the type of surgery performed for the condition.

Objectives To assess the benefits and harms of surgery for patellar tendinopathy in adults.

Search methods We searched the following databases, to 17 July 2018: the Cochrane Central Register of Controlled Trials (CENTRAL) via the Cochrane Library, OVID MEDLINE, OVID Embase, clinical trial registries (www.ClinicalTrials.gov) and the WHO trials portal (www.who.int/ictrp/en/).

Selection criteria We included all randomised controlled trials (RCTs) that compared surgical techniques (open or arthroscopic) with non-operative treatment (including placebo surgery, exercise or other non-surgical modalities) in adults with patellar tendinopathy.

Major outcomes assessed were knee pain, function, quality of life, participant global assessment of success, withdrawal rate, proportion with adverse events and proportion with tendon rupture.

Data collection and analysis Two review authors selected studies for inclusion, extracted trial characteristics and outcome data, assessed the risk of bias and assessed the quality of the evidence using GRADE.

Main results Two trials (92 participants) met our inclusion criteria. Participants in both trials were followed for 12 months. Neither trial compared surgery to placebo surgery. One trial (40 randomised participants) compared open surgical excision with eccentric exercises, and the other compared arthroscopic surgery with sclerosing injections (52 randomised participants). Due to the nature of the interventions, neither the participants or the investigators were blinded to the group allocation, resulting in the potential for performance and detection bias. Some outcomes were selectively not recorded, leading to reporting bias. Overall, the certainty of the evidence from these studies was low for all outcomes due to the potential for bias, and imprecision due to small sample sizes.

Surgery for patellar tendinopathy (jumper’s knee) (Review) 1 Copyright © 2019 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

 Cochrane Trusted evidence. Informed decisions. Library Better health. Cochrane Database of Systematic Reviews

Compared with eccentric exercises, low-certainty evidence indicates that open surgical excision provides no clinically important benefits with respect to knee pain, function or global assessment of success. At 12 months, mean knee pain — measured by pain with standing jump on a 10-point scale (lower scores indicating less pain) — was 1.7 points (standard deviation (SD) 1.6) in the eccentric training group and 1.3 (SD 0.8) in the surgical group (one trial, 40 participants). This equates to an absolute pain reduction of 4% (ranging from 4% worse to 12% better, the minimal clinically important difference being 15%) and a relative reduction in pain of 10% better (ranging from 30%better to 10% worse) in the treatment group. At 12 months, function on the zero- to 100-point Victorian Institute of Sport Assessment (VISA) scale was 65.7 (SD 23.8) in the eccentric training group and 72.9 (SD 11.7) in the surgical group (one trial, 40 participants). This equates to an absolute change of 7% better function (ranging from 4% worse to 19% better) and relative change of 25% better (ranging from 15% worse to 65% better, the minimal clinically important difference being 13%). Participant global assessment of success was measured by the number of people with no pain at 12 months: 7/20 participants in the eccentric training group reported no pain, compared with 5/20 in the open surgical group (risk ratio (RR) 0.71 (95% CI 0.27 to 1.88); one trial, 40 participants). There were no withdrawals, but five out of 20 people from the eccentric exercise group crossed over to open surgical excision. Quality of life, adverse events and tendon ruptures were not measured.

Compared with sclerosing injection, low-certainty evidence indicates that arthroscopic surgery may provide a reduction in pain and improvement in participant global assessment of success, however further studies are likely to change these results. At 12 months, mean pain with activities, measured on a 100-point scale (lower scores indicating less pain), was 41.1 (SD 28.5) in the sclerosing injection group and 12.8 (SD 19.3) in the arthroscopic surgery group (one trial, 52 participants). This equates to an absolute pain reduction of 28% better (ranging from 15% to 42% better, the minimal clinically important difference being 15%), and a relative change of 41% better (ranging from 21% to 61% better). At 12 months, the mean participant global assessment of success, measured by satisfaction on a 100-point scale (scale zero to 100, higher scores indicating greater satisfaction), was 52.9 (SD 32.6) in the sclerosing injection group and 86.8 (SD 20.8) in the arthroscopic surgery group (one trial, 52 participants). This equates to an absolute improvement of 34% (ranging from 19% to 49%). In both groups, one participant (4%) withdrew from the study. Functional outcome scores, including the VISA score, were not reported. Quality-of-life assessment, adverse events, and specifically the proportion with a tendon rupture, were not reported.

We did not perform subgroup analysis to assess differences in outcome between arthroscopic or open surgical excision, as we did not identify more than one study with a common comparator.

Authors' conclusions We are uncertain if surgery is beneficial over other therapeutic interventions, namely eccentric exercises or injectables. Low-certainty evidence shows that surgery for patellar tendinopathy may not provide clinically important benefits over eccentric exercise in terms of pain, function or participant-reported treatment success, but may provide clinically meaningful pain reduction and treatment success when compared with sclerosing injections. However, further research is likely to change these results. The evidence was downgraded two levels due to the small sample sizes and susceptibility to bias. We are uncertain if there are additional risks associated with surgery as study authors failed to report adverse events. Surgery seems to be embedded in clinical practice for late-stage patella tendinopathy, due to exhaustion of other therapeutic methods rather than evidence of benefit.

P L A I N L A N G U A G E S U M M A R Y

Surgery for patella tendinopathy (jumper's knee)

Background

Patella tendinopathy is a painful condition that commonly affects jumping athletes who train a lot, for example those who play olleyballv and basketball. Many people with the condition are unable to continue their chosen sport at the same level of competition or intensity of training. There are many treatments for the condition, the most common of which is a particular type of exercise called eccentric exercise (where the tendon is under tension while the muscle lengthens).

Other treatments for patella tendinopathy include oral and topical analgesia (pain-relief medication taken orally or applied to the skin), various injectables (e.g. corticosteroids) and surgery. Surgery is used if other treatments fail, and is the treatment assessed in this review.

Study characteristics

This Cochrane Review is current to July 2018. We searched online databases for all studies (specifically randomised controlled trials) that compared surgical treatment with non-operative treatment in adults with patellar tendinopathy. We found two studies; they compared open surgical removal to eccentric exercises (one study involving 40 people) and arthroscopic surgery to sclerosing injections (these scar and block the blood vessels supplying nerve fibres to the diseased tendon) (one study involving 56 people). The studies were performed in an outpatient setting in two countries (Norway and Sweden). The majority of people in the studies were male, with a mean age ranging from 27 to 31 years, and mean symptom duration of 24 to 33 months. Trials were conducted without funding (financial support) from industry (medical or device companies), but some authors from the one study received funding from pharmaceutical companies in addition to research funding from non-industry sources.

Key results

Surgery for patellar tendinopathy (jumper’s knee) (Review) 2 Copyright © 2019 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

 Cochrane Trusted evidence. Informed decisions. Library Better health. Cochrane Database of Systematic Reviews

Compared with eccentric exercises, open surgery offered little benefit at 12 months (results for individual outcomes as follows).

Pain (lower scores mean less pain)

Improved by 4% (ranging from 4% worse to 12% better) or by 0.4 points on a scale of zero to 10 points.

People who had surgery rated their pain as 1.3 points.

People who had eccentric exercises rated their pain as 1.7 points.

Global assessment of success (those who reported no pain at 12 months)

10% fewer people had no pain (ranging from 38% less to 18% more), or 10 fewer people out of 100.

Twenty-five out of 100 people had no pain with surgery.

Thirty-five out of 100 people had no pain with eccentric exercises.

Withdrawals

No participants in either group withdrew from the study.

The study did not report on quality-of-life improvements or adverse events (including tendon ruptures).

Compared with sclerosing injections, arthroscopic (keyhole) surgery offered some reduction in pain and improvement in participant global assessment of success at 12 months (results for individual outcomes as follows; further studies are likely to change these results).

Pain (lower scores mean less pain)

Improved by 28% (ranging from 15% to 42% better) or by 28 points on a scale of zero to 100 points.

People who had surgery rated their pain as 12.8 points.

People who had sclerosing injection rated their pain as 41.1 points.

Global assessment of success (participant-reported success, higher score is better)

Improved by 34% (ranging from 19% to 49% better) or by 33.9 points on a scale of zero to 100 points.

People who had surgery rated their pain as 86.8 points.

People who had sclerosing injection rated their pain as 52.9 points.

Withdrawals

One person from each group (4%) withdrew from the study for reasons unrelated to the treatment.

The study did not report on quality-of-life improvements, functional score improvements or adverse events (including tendon ruptures).

Quality of the evidence

We decided the evidence was low-certainty due to flaws in the design of the studies that may over-estimate benefits of treatment. For example, people involved in the study were aware of which treatment they were receiving, the studies selectively reported some results but not others, and there was imprecision in the results due to the small number of participants and trials. Therefore, we are uncertain if surgery has any benefits over eccentric exercises or sclerosing injections for treating patellar tendinopathy in adults. Further studies are likely to change the results.

Surgery for patellar tendinopathy (jumper’s knee) (Review) 3 Copyright © 2019 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

 

Cochrane Trusted evidence. Informed decisions. Library Better health. Cochrane Database of Systematic Reviews 4 3,4 3,4 Comments 4% bet- Absolute change 12% bet- ter (4% worse to 10% ter); relative change 10% better (30% to worse) 7% bet- Absolute change 19% bet- ter (4% worse to 25% ter); relative change 65% better (15% worse to better) Absolute risk difference of 10% less success (38% relative 18% more); less to 29% fewer experi- change at 12 months ence no pain 88% more) (73% fewer to measured Not We cannot estimate com- parative withdrawal rates, as no or cross-overs were surgery to possible from exercise. 1,2 1,2 1,2 1,2 Certainty of the evidence (GRADE)  LOW  LOW  LOW  LOW № of partici- pants (studies) 40 (1 RCT) 40 (1 RCT) 40 (1 RCT) - 40 (1 RCT) (0.27 Relative ef- fect (95% CI) - - RR 0.71 1.88) to - No estimate 7.2 points 0.4 points better 0.4 points (95% CI) * Risk with open surgical excision in the intervention pain The mean was .2 better) (0.4 worse to function was The mean higher 18.8 higher) (4.5 lower to 250 per 1000 658) (95 to measured not No withdrawals or cross-overs surgery possible from were Anticipated absolute effects Risk with eccen- tric exercises pain The mean 1.7 points was func- The mean tion in the con- was trol group 65.7 350 per 1000 measured not over 5/20 crossed surgery to adult participants with patellar tendinopathy open surgical excision eccentric exercises chronic patellar tendinopathy Setting: Intervention: Comparison: Open surgical excision compared to eccentric exercises for patella tendinopathy eccentric exercises for Open surgical excision compared to Patient or population: Outcomes Knee pain 10 (0 is no 0 to from: Scale pain) Follow-up: 12 months Function 100 (100 is 0 to from: Scale function) best Follow-up: 12 months Participant global assess- ment of success (People who perceived their as none) pain Follow-up: 12 months Quality of life Withdrawal rate S U M A R Y O F I N D G tendinopathy patella for exercises eccentric to compared excision Open surgical the main comparison. Summary of findings for

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Cochrane Trusted evidence. Informed decisions. Library Better health. Cochrane Database of Systematic Reviews ran- RCT: Comments of the intervention (and Not estimable Not reported, unclear if Not mea- this outcome was sured here is a possibility that it here (values were 3.9 points on a zero- 3.9 points were (values te of effect Certainty of the evidence (GRADE) 1,2 ct relative effect Bahr 2006  VERY LOW - linically important benefit. For adverse events, benefit. For important linically rom rom № of partici- pants (studies) 40 (1 RCT) - Relative ef- fect (95% CI) number needed to treat for an additional harmful outcome; for treat number needed to NNTH: - Victorian Institute of Sport Assessment (95% CI) VISA: * Risk with arthroscopic surgery One participant developed chronic quadriceps pain reported Not Visual Analogue Scale; Visual Analogue Scale; VAS: Anticipated absolute effects Risk with sclerosing injection (and its 95% confidence interval) is based on the assumed risk in the comparison group and the on the assumed risk in comparison group 95% confidence interval) is based (and its None reported Not number needed to treat for an additional beneficial outcome; for treat number needed to risk ratio; RR: NNTB: adult participants with patellar tendinopathy We are moderately confident in the effect estimate: The true effect is likely to be close to the estimate of effect, but t be close to moderately confident in the effect estimate: The true is likely to We are We have very the estima be substantially different from little confidence in the effect estimate: The true is likely to We are very We are that of the estimate effect confident that the true effect lies close to Our confidence in the effect estimate is limited: The true effect may be substantially different from the estimate of effe Our confidence in the effect estimate is limited: The true may be substantially different from arthroscopic surgery sclerosing injection chronic patellar tendinopathy confidence interval; The risk in the intervention group Very low certainty: low Very its 95% CI). its CI: domised controlled trial; Moderate certainty: Setting: Intervention: Comparison: Adverse event Tendon rupture * of evidence grades Working Group GRADE High certainty: patella tendinopathy sclerosing injection for compared to Arthroscopic surgery Patient or population: Outcomes substantially different certainty: Low Downgraded one level for significant detection bias and reporting bias bias and reporting detection significant one level for Downgraded or rule out a c confirm do not intervals a single small trial, confidence from — evidence Imprecision one level for Downgraded f group exercises baseline in the eccentric at divided by mean difference) (mean change as absolute calculated changes Relative for any outcome. differences between-group important no clinically were as there calculated not NNNTB or NNTH were downgraded twice as only one event was reported in one group reported as only one event was twice downgraded

to 10-point VAS for pain; and 29 points on a zero- to 100-point VISA scale) to on a zero- and 29 points pain; for 10-point VAS to 1 2 3 4 tendinopathy patella for injection sclerosing to compared surgery Arthroscopic Summary of findings 2.

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Cochrane Trusted evidence. Informed decisions. Library Better health. Cochrane Database of Systematic Reviews , 3 4 NNTB 2 (1 to 4) Absolute dif- ference 28% better (15% 42% bet- to ter); relative 41% change better (21% to 61% better) reported Not Absolute im- provement of 34% (19% to 49%) measured Not related Not treatment to (pregnancy) reported, Not unclear if this outcome was measured reported, Not unclear if this outcome was measured 1,2 of the intervention (and Visual Analogue Scale 1,2 1,2 here is a possibility that it here VAS:  LOW -  LOW -  VERY LOW - - relative effect risk ratio; RR: 50 (1 RCT) - 50 (1 RCT) 40 (1 RCT) ------randomised controlled trial; RCT: The mean pain was 28.3 points better 28.3 points was pain The mean 41.8 (14.8 to in the intervention group better). points reported Not 33.9 patient satisfaction was The mean better). 49.1 points better (18.7 to points measured Not 1 event, no reliable estimate reported Not reported Not Mean pain was 41.1 was pain Mean points. reported Not satisfaction Mean 52.9 points. was measured Not 1 event reported Not reported Not (and its 95% confidence interval) is based on the assumed risk in the comparison group and the on the assumed risk in comparison group 95% confidence interval) is based (and its number needed to treat for an additional beneficial outcome; for treat number needed to NNTB: We are moderately confident in the effect estimate: The true effect is likely to be close to the estimate of effect, but t be close to moderately confident in the effect estimate: The true is likely to We are We are very We are that of the estimate effect confident that the true effect lies close to confidence interval; The risk in the intervention group GRADE Working Group grades of evidence grades Working Group GRADE High certainty: Moderate certainty: substantially different its 95% CI). its CI: Knee pain 100 (0 is no pain) 0 to from: Scale Follow-up: 12 months Function Participant global assessment of success 100 (higher is 0 to from: Scale satisfaction) greater Follow-up: 12 months Quality of life Withdrawal rate Adverse event Tendon rupture *

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Cochrane Trusted evidence. Informed decisions. Library Better health. Cochrane Database of Systematic Reviews (value was 69 points on a 69 points was (value te of effect ct Willberg 2011 Willberg from from linically important benefit. For withdrawal rate, withdrawal benefit. For important linically We have very the estima be substantially different from little confidence in the effect estimate: The true is likely to Our confidence in the effect estimate is limited: The true effect may be substantially different from the estimate of effe Our confidence in the effect estimate is limited: The true may be substantially different from Very low certainty: low Very Low certainty: Low Downgraded one level for significant detection bias and reporting bias bias and reporting detection significant one level for Downgraded or rule out a c confirm do not intervals a single small trial, confidence from — evidence imprecision one level for Downgraded group injection baseline in the sclerosing at divided by mean difference) (mean change as absolute calculated changes Relative reported outcomes or no dichotomised reported, was of satisfaction measure as no baseline change relative calculate Unable to zero- to 100-point VAS for pain) for 100-point VAS to zero-

downgraded twice as only one event per group reported as only one event per group twice downgraded 1 2 3 4

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B A C K G R O U N D as it contracts) are used. In the case of knee tendinopathy, eccentric exercises typically include decline squat training or Description of the condition similar exercises (Larsson 2012; Malliaras 2013).

Patellar tendinopathy is an overuse condition that commonly Approximately 10% of athletes with patellar tendinopathy, usually affects athletes, with an overall incidence of 14% in one study Lian( those in the latter stages of the condition for whom non-surgical 2005). Patellar tendinopathy is more common in jumping sports, interventions have failed, undergo surgery (Ogon 2006). Surgery with up to 40% incidence in volleyball players (Ferretti 1986); hence, may be performed with an open incision, or arthroscopically (with Blazina coined the term 'jumper's knee' in his original description an endoscope or illuminated optical tubing device, via a small of the condition (Blazina 1973). The prognosis is poor: one report incision or keyhole). Procedures include surgical debridement or suggests that more than one-third of athletes who seek treatment excision of the degenerated areas of the tendon; drilling of the do not return to sport within six months (Cook 1997), and another lower pole of the patella bone at the site of tendon attachment study reported that up to 53% of athletes retire from sport due to to stimulate new blood flow and promote healing (Blazina 1973; the condition, compared to 7% of athletes who retire without the Romeo 1999); and tenotomy, which involves an incision to expose condition (Kettunen 2002). the tendon, followed by cutting through or disconnecting the tendon to allow for a greater range of movement of the tendon and 'Jumper’s knee' is a broader term than patellar tendinopathy and joint (Khan 1999); or a combination of procedures. includes people with pain at the quadriceps insertion of the tendon (25% of cases), the insertion at the distal (inferior) pole of the How the intervention might work patella (knee cap) (65%), and the insertion at the tibial tubercle (raised area of bone over the upper tibia) (10%) (Ferretti 1985). There are different purported modes of action depending on the However, patellar tendinopathy is limited to symptoms where the type of surgical intervention. During surgical debridement, the patellar tendon (also known as the patellar ligament) inserts at the surgeon removes the diseased portion of the tendon. Drilling of the distal pole of the knee cap (Ferretti 1985). bone at the site of tendon attachment is thought to stimulate a healing response by inducing blood flow to the area (Blazina 1973; The condition was previously called tendonitis, implying it Romeo 1999). Tenotomy involves cutting through the tendon, and is is associated with inflammation, but histology shows it is thought to 'release' the tendon to allow greater range of movement degenerative rather than inflammatory. It is characterised by through the tendon and muscle (Khan 1999). How surgery improves degeneration, cell death and micro-tears in the tendon, along the function of the patellar tendon is not well understood, as with evidence of formation of new blood vessels (Khan 2002). there seems to be little correlation between the appearance of The diagnosis is usually clinical but ultrasound shows thickening abnormalities on imaging of the tendon and clinical assessment via of the tendon (Mourad 1988), and both ultrasound and magnetic functional scores after surgery Khan( 1999). resonance imaging (MRI) scanning indicate abnormalities at the proximal patellar tendon attachment and blurry ligament margins Why it is important to do this review (Khan 1996). Surgery is usually offered for patella tendinopathy after failure The primary classification system used to grade the severity of of medical and physical therapies, but there is variation in patella tendinopathy was formalised by Blazina, who divided the the type of surgery performed for the condition, and little condition into phases (Blazina 1973). This provided a qualitative consensus on the benefits of surgery (Figueroa 2016; Kaeding description of the clinical progression of the disease. Phase 1 is pain 2006; Khan 2016). Indeed, the clinical benefit of surgery has after exercise, phase 2 is characterised by pain that is present at the been questioned; a randomised controlled trial reported little beginning and end of activity but absent after ‘warm up’, and phase difference in outcome between participants who underwent 3 is pain during and after activity (Blazina 1973). Phase 4 was a later surgery compared with those who received eccentric exercise addition by Roels and others which represents complete tendon training, and both treatment groups reported improvement over rupture (Roels 1978). the 12-month follow-up (Bahr 2006). However, large case series reporting the utility of surgery for the condition continue to be To better quantify severity and response to treatment, the Victorian published (Brockmeyer 2015), and review articles summarising Institute of Sport Assessment (VISA) scale was developed. Designed evidence from case series also conclude that surgery is beneficial in 1998, it is a series of eight questions with a total score out of (Figueroa 2016; Khan 2016). There is no current systematic review 100, and a higher score represents fewer symptoms. Examples of that summarises and appraises the quality and strength of mean scores are 95 (standard deviation (SD) 8) for asymptomatic evidence from randomised controlled trials comparing surgical and individuals; 55 (SD 12) for those with the disease participating in non-surgical interventions. sport; 22 (SD 17) as a preoperative score; 49 (SD 15) for six-month postoperative recovery; and 75 (SD 17) for 12-month postoperative O B J E C T I V E S recovery (Visentini 1998). To assess the benefits and harms of surgery for patella Description of the intervention tendinopathy in adults. Non-surgical treatments for patellar tendinopathy include The major outcomes were pain, function, quality of life, participant reduction in sporting and other activity, exercise, anti- global assessment of success, withdrawal rate, total adverse events inflammatory drugs, taping, massage, physiotherapy modalities and tendon rupture. The minor outcome was return to sport. and injection therapies; there is limited evidence or consensus on optimal treatment (Cook 2001). Most commonly, exercise strength in particular, eccentric exercises (when the muscle lengthens Surgery for patellar tendinopathy (jumper’s knee) (Review) 8 Copyright © 2019 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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M E T H O D S Searching other resources

Criteria for considering studies for this review We checked the reference lists of all primary studies and review articles for potential additional studies. Types of studies Data collection and analysis We included studies described as randomised controlled trials (RCTs). We included studies reported as full text, those published Selection of studies as abstract only and unpublished data. TWe applied no language or Two review authors (MD, AP) independently screened titles and date restrictions on the search. abstracts of all potentially relevant studies from the search for Types of participants inclusion and coded them as 'retrieve' (eligible or potentially eligible/unclear) or 'do not retrieve'. We retrieved the full-text We included trials of adults with a diagnosis of patella reports and two review authors (MD, AP) independently screened tendinopathy, as defined in the trials. the full text, identified studies for inclusion and identified and recorded reasons for exclusion of the ineligible studies. We resolved Types of interventions any disagreement through discussion or, if required, we consulted Trials were eligible if they compared surgical techniques (open or a third person (IH). We identified and excluded duplicates and arthroscopic) with placebo surgery, exercise or other non-surgical collated multiple reports of the same study so that each study, modalities. rather than each report, was the unit of interest in the review. We recorded the selection process in sufficient detail to complete a Types of outcome measures PRISMA flow diagram (PRISMA Group 2009, prisma-statement.org/ PRISMAStatement/Default.aspx) and Characteristics of excluded Major outcomes studies table. • Knee pain: mean overall pain, assessed by visual analogue scale (VAS), numerical or categorical rating scales or other measures. Data extraction and management • Function: mean function, assessed by Victorian Insitute of Sport We used a data collection form for study characteristics and Assessment (Visentini 1998) or Lysholm or other region-specific outcome data. Data were independently extracted by two review or condition-specific scores. authors (MD and AP) and disagreements settled by discussion or • Health-related quality of life: overall quality-of-life score (e.g. referral to the senior author (IH). We extracted the following study SF-36, EQ5D, EQ-VAS). characteristics. • Participant global assessment of success, as measured by • Methods: study design, total duration of study, details of any a participant-reported global impression of clinical change 'run-in' period, number of study centres, location, study setting, (improvement), or similar measure. withdrawals and year of study. • Proportion of withdrawals. • Participants: number, mean age, age range, sex, socioeconomic • Proportion with adverse events (any). status, disease duration, severity of condition, diagnostic • Proportion with tendon rupture. criteria, important condition-specific and general health baseline data, inclusion criteria and exclusion criteria. Minor outcomes • Interventions: intervention, comparison, concomitant • Return to sport. medications, concomitant physical treatments and excluded treatments. Time points • Outcomes: primary and secondary outcomes specified and Follow-up times were expected to be between three months and collected and time points reported. two years. We planned to extract data on pain, function, quality • Characteristics of the design of the trial, as outlined below in of life, global success and adverse events at six months and 12 Assessment of risk of bias in included studies. months. If data were reported at multiple time points within each • Notes: funding for trial and notable declarations of interest of of these periods, we planned to extract data at the latest possible trial authors. time point up to six months and up to 12 months. Two review authors (MD, AP) independently extracted the outcome Search methods for identification of studies data from the included studies. We extracted the number of Electronic searches events and the number of participants per treatment group for dichotomous outcomes, and means and standard deviations We searched the Cochrane Central Register of Controlled Trials and number of participants per treatment group for continuous (CENTRAL), Ovid MEDLINE and Ovid Embase. We also conducted a outcomes. We noted in the Characteristics of included studies table search of ClinicalTrials.gov (www.ClinicalTrials.gov) and the WHO if outcome data were not reported in a usable way and when trials portal (www.who.int/ictrp/en/). We searched all databases data were transformed or estimated from a graph. We resolved from their inception until 17 July 2018 and we imposed no disagreements by consensus or by involving a third person (IH). restriction on language of publication. See Appendix 1 for the One review author (MD) transferred the data into the Review MEDLINE search strategy; Appendix 2 for CENTRAL, Appendix 3 for Manager 5 file (RevMan 2014). We confirmed the accuracy of data by Embase and Appendix 4 for trial registries. comparing those presented in the systematic review with the study

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 Cochrane Trusted evidence. Informed decisions. Library Better health. Cochrane Database of Systematic Reviews reports. We used Web Plot Digitizer website to extract data from We presented the figures generated by the 'Risk of bias' tool to graphs or figures. These data were also extracted in duplicate. provide summary assessments of the risk of bias.

We applied the following a priori decision rules to select which data Assesment of bias in conducting the systematic review to extract in the event of multiple outcome reporting. We conducted the review according to the published protocol and • Pain: overall pain was selected preferentially over pain related to report any deviations from it in Differences between protocol and activity, followed by pain at rest. We preferentially selected pain review. on a VAS scale over pain reported on numerical or categorical rating scales, and over pain reported on other scales, such as a Measures of treatment effect subscore of a knee score. We analysed dichotomous data as risk ratios or Peto odds ratios • Knee functional outcome scores: VISA score was preferred, when the outcome was a rare event (less than 10%), and used 95% followed by Lysholm Knee Score, Knee injury and Osteoarthritis confidence intervals (CIs). Continuous data were analysed as mean Outcome score (KOOS), Western Ontario and McMaster difference (MD) or standardised mean difference (SMD), depending Universities Osteoarthritis Index (WOMAC) and Oxford Knee on whether the same scale was used to measure an outcome, and scores. 95% CIs. We entered data presented as a scale with a consistent • If both final values and change-from-baseline values were direction of effect across studies. reported for the same outcome, we preferentially extracted change-from-baseline values. When different scales were used to measure the same conceptual outcome (e.g. disability), SMDs were calculated, with • If both unadjusted and adjusted values for the same outcome corresponding 95% CIs. SMDs were back-translated to a typical were reported, we preferentially extracted adjusted values. scale (e.g. zero to 10 for pain) by multiplying the SMD by a typical • In accordance with Consolidated Standards Of Reporting Trials among-person standard deviation (e.g. the standard deviation (CONSORT) guidelines, we reported on both intention-to-treat of the control group at baseline from the most representative and per-protocol analysis, using the per-protocol to explore trial), in accordance with Chapter 12 of theCochrane Handbook for 'efficacy' of the intervention versus intention-to-treat to reflect Systematic Reviews of Interventions (Schünemann 2017b). the 'effectiveness' of the intervention. • If there were multiple time points, we extracted outcomes If return to sport was measured at intervals outside the three-, six- reported up to six months and up to 12 months. or 12-month time points, we analysed time-to-event data as hazard ratios. Rate data were to be analysed using Poisson methods. Main planned comparisons In Effects of interventions, Summary of findings for the main • Surgery versus placebo. comparison and Summary of findings 2, we provide the absolute • Surgery versus exercise which is a commonly used first-line per cent difference and the relative per cent change from baseline. therapy. Where the outcome showed a clinically significant difference, we • Surgery versus other non-operative interventions, including but also provide the number needed to treat for an additional beneficial not limited to glucocorticoid injection; other injections including outcome (NNTB) or number needed to treat for an additional autologous blood products, stem cells and sclerosing agents; or harmful outcome (NNTH). For dichotomous outcomes, the NNTB pharmacological treatments (we planned to present the results or NNTH was calculated from the control group event rate and by common comparisons). the relative risk, using the Visual Rx NNT calculator (Cates 2008). The NNTB or NNTH for continuous measures was calculated using Assessment of risk of bias in included studies the Wells calculator (available at the Cochrane Musculoskeletal editorial office). Two review authors (MD, AP) independently assessed the risk of bias for each study using the criteria outlined in the Cochrane When interpreting results, we assumed a minimal clinically Handbook for Systematic Reviews of Interventions (Higgins 2017). important difference of 1.5 points on a 10-point pain scale or 15 Risk of bias included selection, performance, detection, attrition points on a 100-point scale (Hawker 2011); and 13 points on the and reporting bias. We resolved any disagreements by discussion zero-to-100 VISA scale (Hernandez-Sanchez 2014). or by involving another review author (IH). For dichotomous outcomes, the absolute risk difference was We considered blinding separately for different key outcomes, calculated using the risk difference statistic in Review Manager where necessary (e.g. for unblinded outcome assessment, risk of software (RevMan 2014), and the result expressed as a percentage. bias for tendon rupture may be different than for a participant- For continuous outcomes, the absolute benefit was calculated reported pain scale). We also considered the impact of missing data as the improvement in the intervention group minus the by key outcomes. improvement in the control group, in the original units, expressed as a percentage. Where information on risk of bias was obtained from unpublished data or correspondence with an author, we noted this in the 'Risk The relative per cent change for dichotomous data was calculated of bias' table. as the risk ratio minus one, expressed as a percentage. For continuous outcomes, the relative difference in the change from When considering treatment effects, we took into account the risk baseline was calculated as the absolute benefit divided by the of bias for the studies that contributed to that outcome. baseline mean of the control group, expressed as a percentage.

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Unit of analysis issues Assessment of reporting biases Where multiple trial arms were reported in a single trial, we We planned to create and examine a funnel plot to explore possible included only the relevant arms. We planned to halve the control small-study biases. In interpreting funnel plots, we planned to group if two comparisons (e.g. arthroscopic surgery versus placebo examine the different possible reasons for funnel plot asymmetry and open surgery versus placebo) were combined in the same as outlined in Sterne 2017. If we are able to pool more than meta-analysis. 10 trials, we planned to undertake formal statistical tests to investigate funnel plot asymmetry, and planned to follow the Dealing with missing data recommendations in Sterne 2017. We contacted investigators or study sponsors in order to verify key To assess outcome reporting bias, we checked trial protocols study characteristics and obtain missing numerical outcome data, against published reports. For studies published after 1 July where possible (e.g. when a study was identified as abstract only 2005, we screened the WHO trial search at the International or when data were not available for all participants). Where this Clinical Trials Registry Platform of the World Health Organization was not possible, and the missing data were thought to introduce (http://apps.who.int/trialssearch/) for the a priori trial protocol. We serious bias, we explored the impact of including such studies in the evaluated whether selective reporting of outcomes was present. overall assessment of results by a sensitivity analysis. Data synthesis For dichotomous outcomes (e.g. number of withdrawals due to adverse events), we calculated the withdrawal rate using We planned to undertake meta-analyses only where this would be the number of participants randomised in the group as the meaningful, i.e. if the treatments, participants, and the underlying denominator. clinical question were similar enough for pooling to make sense. We planned to use a random-effects model. For continuous outcomes (e.g. mean change in pain score), we calculated the MD or SMD based on the number of participants GRADE and 'Summary of findings' tables analysed at that time point. We planned to use the number of We created a 'Summary of findings' table using the following randomised participants in each group at baseline, if the number of outcomes: pain; knee function; quality of life; participant global participants analysed was not presented for each time point. assessment of success; withdrawal rate; adverse events (total); and Where possible, we computed missing standard deviations from tendon rupture. other statistics such as standard errors, CIs or P values, according The comparison in the first 'Summary of findings' table is eccentric to the methods recommended in the Cochrane Handbook for exercise, followed by pooled non-operative interventions in the Systematic Reviews of Interventions (Li 2019). If we could not second table. The main time point is 12 months. calculate standard deviations, we imputed them (e.g. from other studies in the meta-analysis) (Li 2019). Two review authors(MD, AP) independently assessed the certainty of the evidence. We used the five GRADE considerations (study Assessment of heterogeneity limitations, consistency of effect, imprecision, indirectness, and Clinical and methodological diversity were assessed in terms of publication bias) to assess the quality of a body of evidence participants, interventions, outcomes, and study characteristics for as it relates to the studies which contribute data to the meta- the included studies, to determine whether a meta-analysis was analyses for the prespecified outcomes, and reported the certainty appropriate. This was done by observing the data in the data of evidence as high, moderate, low, or very low. We considered extraction tables. Statistical heterogeneity was assessed by visual the following criteria for upgrading the certainty of evidence, if inspection of the forest plot to assess for obvious differences in appropriate: large effect, dose-response gradient and plausible results between the studies, and by using the I2 and Chi2 statistical confounding effect. We used the methods and recommendations tests. described in section 8.5 and 8.7, and chapters 11 and 12, of the Cochrane Handbook for Systematic Reviews of Interventions As recommended in Deeks 2017, we interpreted I2 values as follows: (Higgins 2017; Schünemann 2017a; Schünemann 2017b). We 0% to 40% 'might not be important'; 30% to 60% may represent used GRADEpro GDT software to prepare the 'Summary of 'moderate' heterogeneity; 50% to 90% may represent 'substantial' findings' tables (GRADEpro GDT 2015). We justified all decisions to heterogeneity; and 75% to 100% may represent 'considerable' downgrade or upgrade the certainty of studies using footnotes and heterogeneity. As noted in the Cochrane Handbook for Systematic comments to aid the reader's understanding of the review, where Reviews of Interventions, we understood that the importance of I2 necessary. We provided the NNTB or NNTH, and the absolute and depends on the magnitude and direction of effects and the strength relative per cent change, in the 'Comments' column of the tables, of evidence for heterogeneity. as described in Measures of treatment effect.

The Chi2 test values were interpreted as follows: a P value of 0.10 or Subgroup analysis and investigation of heterogeneity less indicates evidence of statistical heterogeneity. We planned to carry out the following subgroup analyses, for the If we identified substantial heterogeneity (greater than 50%), we outcomes knee pain and function. planned to report it and investigate possible causes by following • the recommendations in Deeks 2017. Open surgery versus arthroscopic surgery. • Secondary analysis combining non-operative comparators.

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We planned to use the formal test for subgroup interactions • Detection bias: we planned to remove trials with unclear or in Review Manager 5 (RevMan 2014) and to use caution in the inadequate blinding of the participants from the meta-analysis. interpretation of subgroup analyses, as advised in Deeks 2017. R E S U L T S Sensitivity analysis Description of studies We planned to carry out sensitivity analyses to investigate the robustness of the treatment effect for pain and function in terms of Results of the search selection and detection biases. The search strategy identified 225 unique citations. After screening • Selection bias: we planned to remove trials at risk of selection titles and abstracts, we excluded 217 studies and assessed the full bias (i.e. with inadequate or unclear allocation concealment) text of eight citations. Six of these were excluded (reasons listed from the meta-analysis. below), and two studies met the inclusion criteria. We did not identify any ongoing studies or studies awaiting classification. The results of the search are presented in Figure 1.

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Figure 1. Study flow diagram.

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Figure 1. (Continued)

Included studies One study (Bahr 2006) reported similar levels of function between the open surgical excision group and the eccentric exercises group Trial design, setting and characteristics at baseline (scores of 31/100 and 29/100, respectively). The other We included two RCTs in the review. Both were parallel study (Willberg 2011) did not report on functional outcomes. trials. Participants, inclusion and exclusion criteria, interventions, comparators and outcomes are described in the Characteristics Interventions of included studies table, along with any clinical characteristics a Surgery was performed differently in the two studies. In one reader (i.e. patient or surgeon) might wish to know (e.g. so they can study, open surgical excision was carried out by two orthopaedic see whether the characteristics of participants in the trial match surgeons, whereas the details of who performed the arthroscopic their own). Participants in both trials were followed for a total of 12 surgery in the other study not disclosed. months. One trial compared open surgical excision with eccentric exercises (Bahr 2006), and the other compared arthroscopic surgery Open surgical excision involved a 5 cm longitudinal midline with sclerosing injections (Willberg 2011). No errata or retractions incision from the inferior pole of the patella distally. A tourniquet were noted at the time of the search. was not used. The paratenon was split longitudinally and any pathologic paratenon tissue was removed. The tendon was split Trial participants longitudinally in the midline to expose the deepest layers and The two trials included a total of 92 randomised participants; trial all tissue that appeared abnormal was removed, or if not seen sizes varied from 40 to 52 participants. In general, the inclusion macroscopically the area calculated from the MRI was removed. criteria for both trials were similar and included a clinical history, Once the sutures were removed the participants were exposed examination and imaging findings consistent with a presentation to the same physiotherapist and eccentric exercises as the non- of patella tendinopathy, patient complaints of pain and tenderness operative group (Bahr 2006). at the inferior pole of the patella. In both studies participants Arthroscopic surgery was performed under local anaesthetic, had failed a minimum of three months of non-surgical treatment, using anterolateral and anteromedial portals. No tourniquet was including rest, analgesia and physical therapy. used. The patella tendon insertion into the patella was identified Across both trials the majority of participants were male (less than following a routine arthroscopic examination of the knee. A 4.5 10% of participants in each study were female) with a mean age of mm shaver was utilised to destroy only the region with high blood 26 to 31 years. Symptom duration varied but there was a mean of flow and nerves adjacent to the tendinosis changes on the dorsal 20 to 30 months' duration in symptoms. side of the tendon identified with ultrasound. No tendon tissue was resected and the Hoffa (Infrapatellar) fat pad was saved. Portals One study did not report training volume at baseline (Willberg were closed with tape. No information was given on who performed 2011). Similar loads were reported in Bahr 2006, with means of 12.2 the surgeries. Postoperatively, participants were allowed to weight hours per week in the open surgical excision group compared with bear as tolerated; from two weeks, gradual increase in loading of 11.2 hours per week in the eccentric exercises group. the tendon as tolerated was allowed, with no specific instructions on what exercises to do. This was the same as the sclerosing The studies used different scales for measuring pain; in one study injection group (Willberg 2011). the surgical group had a baseline score of 4.3/10 pain with jumping, compared to 3.9/10 in the eccentric exercises group. In the other Non-operative comparisons involved eccentric exercises and study the surgical group had higher baseline pain levels, with sclerosing injections. Eccentric exercises were performed by the activity-related pain scores of 76.5/100 compared to 69.0/100 in the participants themselves with weekly supervision provided by sclerosing injection group. It is not clear what these activities were, the same physiotherapist. The exercises involved using a 25- and therefore we cannot draw conclusions as to why the difference degree decline board at home, where the downward (eccentric) existed. component was performed on the affected leg and the upward (concentric) component was performed on the asymptomatic leg.

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The participant was instructed to perform the squat to 90 degrees continuous outcome. The dichotomous outcome looked at the with the back in a vertical position. The participant was instructed proportion of participants with no pain at 12 months, whereas the to take two seconds for the eccentric component. The exercises continuous outcome was a self-report VAS on an 11-point scale involved twice-daily sessions of three sets of 15 repetitions for from -5 to +5, with positive scores indicating an improvement in the a total duration of 12 weeks, with weekly supervision by a condition. physiotherapist. No warm-up was performed (Bahr 2006). The other study (Willberg 2011) also utilised a VAS, however Sclerosing injections were performed using Polidocanol. A 0.7 mm it was a zero- to 100-point scale, with higher scores indicating x 50 mm needle, connected to a 2 mL syringe, was utilised. Volumes better satisfaction with treatment. The study reported the mean of 0.1 mL to 0.2 mL were injected into the regions with local satisfaction score. neovascularisation/high blood flow dorsal to the proximal patellar tendon under ultrasound guidance. A maximum of three injections Withdrawal rate were given at six-week intervals. All injections were performed Both studies included the number of participants who withdrew by the same, single sonographer. Post-injection, participants were and the qualitative reason for the withdrawal. allowed to weight bear as tolerated; from two weeks, gradual increase in loading of the tendon as tolerated was allowed, with no Outcomes not measured specific instructions on what exercises to do. This was the same as Neither study measured participants' quality of life or adverse the arthroscopic surgery group (Willberg 2011). events, including the proportion of participants who developed a Outcomes tendon rupture. Personal communication with the corresponding author of Bahr 2006 indicated that there were no tendon ruptures Pain noted in clinical follow-up. Attempts to contact the authors of All studies assessed at least one measure of pain, but measurement Willberg 2011 failed, so we cannot comment on whether there were varied across trials. In one study, knee pain was measured by pain any tendon ruptures or not. The authors of Willberg 2011 directly with standing jump (Bahr 2006). This was recorded on a zero- to 10- commented that they chose not to use a functional outcome (like point VAS at 12 months only. A lower score meant less pain. The VISA) as they felt it was not reflective of the improvement gained in other study (Willberg 2011) utilised a visual analogue scale for pain, the trial participants, as they were not elite athletes. with values of zero to 100, where a lower score meant less pain. Excluded studies Function Six studies were excluded after intially being screened, as they Only one of the two studies (Bahr 2006) reported functional failed to meet the inclusion criteria. Three studies were not RCTs outcomes. It utilised the Victorian Institute of Sport Assessment (Coleman 2000; Cuellar 2007; Sunding 2015), two studies were (VISA) score for patella tendinopathy to measure functional review articles (Gaida 2011; MarcheggianiMuccioli 2013), and one response. The VISA score is a patient-reported outcome score on study was of the wrong intervention (Dragoo 2011). a zero- to 100-point scale, with higher scores indicating better function. The second study (Willberg 2011) appeared to measure Risk of bias in included studies the VISA score, but did not report it at baseline or follow-up. The 'Risk of bias' assessment for each study is reported in the Characteristics of included studies table and summarised in Figure Participant global assessment of success 2 and Figure 3. Both studies measured participant global assessment of success. One study (Bahr 2006) did this using both a dichotomous and

Figure 2. Risk of bias graph: review authors' judgements about each risk of bias item presented as percentages across all included studies.

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Figure 3. Risk of bias summary: review authors' judgements about each risk of bias item for each included study.

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Allocation Benefits One trial (Bahr 2006) described adequate allocation concealment 1. Open surgical excision compared with eccentric exercises (through sealed opaque envelopes) and random sequence Bahr 2006 compared open surgical excision with eccentric exercises generation to intervention or comparator prior to the start of the in 40 participants (20 participants in each group). At the completion study, so was likely to be at low risk of selection bias. of follow-up (12 months), five of the 20 participants from the Methodology for sequence generation was not provided in Willberg eccentric exercises group had crossed over to the surgical group. 2011, and although concealed envelopes were used for allocation, An intention-to-treat analysis was performed to include these the participants selected their own envelope. Therefore, there was participants in the final comparison. The five participants who a possibility of selection bias. crossed over from the eccentric exercises group to the open surgery group had no improvement in baseline values, i.e. these Blinding participants experienced no improvement after three months of eccentric exercises, and again no improvement 12 months after We assessed both studies as being at high risk of both performance surgery. and detection bias. The participants were not blinded with regard to the group allocation, therefore there was potential for detection The certainty of evidence was low for knee pain, function and global bias for self-reported outcomes (pain, function, global evaluation) assessment of success (downgraded for imprecision, detection and and performance-related outcomes due to knowledge of the reporting bias) and the results found that open surgical excision allocated interventions by participants. The assistant collecting the provides no clinically important benefits for these outcomes. outcome scores was blinded to group allocation, however the data Quality of life, adverse events and tendon ruptures were not were recorded by participants who were not blinded and therefore reported. Major outcomes are reported in Summary of findings for there is a high risk of detection bias. the main comparison.

Incomplete outcome data Knee pain Attrition bias was minimised in both studies. In Bahr 2006, five out At 12 months, mean pain scores with standing jump (measured of 20 participants from the eccentric exercises group crossed over on a 10-point VAS scale, where a lower score indicates less pain) to the open surgical excision group, however the final score prior were 1.7 (SD 1.6) in the eccentric training group and 1.3 (SD 0.8) to surgery was carried over to the 12-month follow-up. In the other in the surgical group (one study, 40 participants). This equates study (Willberg 2011), only one out of 26 participants from both to a mean difference of -0.4 points (95% CI -1.2 to 0.4), or an groups withdrew from the study due to reasons unrelated to the absolute pain reduction of 4% (4% worse to 12% better, the minimal treatment. clinically important difference being 1.5%) and a relative change in pain of 10% better (30% better to 10% worse) in the treatment Selective reporting group. As the 95% CIs included both clinically significant and non- We judged both studies to have a high risk of reporting bias. significant values, there was no clinically important difference in Both failed to report any measures of quality-of-life assessment pain between eccentric training and surgery at 12 months (low- or adverse events, including the presence or absence of tendon certainty evidence). Pain at six months was not reported. Analysis ruptures. One study (Willberg 2011) actively chose not to report 1.1 validated functional scores (VISA scores), although it may have Function collected these data. At six months, mean function on the 100-point VISA scale (where Other potential sources of bias a higher score indicates better function) was 55.7 (SD 16.6) in the There were no other sources of bias. Cointerventions, including eccentric training group and 58.9 (SD 22.7) in the surgical group analgesics for pain relief, were allowed freely in both treatment (one study, 40 participants). This equates to a mean difference of groups. 3.2 points (95% CI -9.5 to 16.0), an absolute change of 3% better function in the treatment group (9.5% worse to 16% better, the Effects of interventions minimal clinically important difference being 13%). See: Summary of findings for the main comparison Open surgical At 12 months, mean function on the VISA scale was 65.7 (23.8) in excision compared to eccentric exercises for patella tendinopathy; the eccentric training group and 72.9 (11.7) in the surgical group. Summary of findings 2 Arthroscopic surgery compared to This equates to a mean difference of 7.2 points (95% CI -4.5 to 18.8), sclerosing injection for patella tendinopathy an absolute change of 7% better function (4% worse to 19% better) and a relative change of 25% better function (15% worse to 65% Meta-analysis better) in the treatment group. Low-certainty evidence showed The interventions in the trials were considered too diverse to there was no clinically important difference in function between pool outcomes in a meta-analysis: Bahr 2006 compared open eccentric training and surgery; the 95% CIs indicate that a clinically surgical incision of the patellar tendon, followed by rehabilitation important change cannot be confirmed or excluded. Analysis 1.2 progressing to eccentric exercise, with eccentric exercise alone; Participant global assessment of success Willberg 2011 compared arthroscopic shaving of the tendon with sclerosing injection. Global assessment of success was assessed as a dichotomous and continuous variable.

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Success, defined as no pain at 12 months, was achieved in 7/20 satisfaction) was 52.9 (SD 32.6) in the sclerosing injection group and participants (or 350 per 1000) in the eccentric exercises group and 86.8 (SD 20.8) in the arthroscopic surgery group. This equates to a 5/20 (or 250 per 1000) in the surgical group: risk ratio (RR) 0.71 mean improvement of 33.9 points (95% CI 18.7 to 49.1), an absolute (95% CI 0.27 to 1.88; one trial, 40 participants). This equates to an improvement of 34% (19% better to 49% better) in the treatment absolute change of 10% less success (38% less to 18% more) and a group (one study, 50 participants). This is likely a clinically relative change of 29% less success (73% fewer to 88% more) in the important difference between groups (assuming 10% is clinically treatment group. Analysis 1.3 important), however the evidence is of low certainty.Analysis 2.2

At six months, the mean global assessment of success (on a scale of Proportion of withdrawals -5 to +5, where a positive score indicates greater perceived benefit) The withdrawal rate was the same in each treatment arm (1/26, or was 2.0 (SD 1.3) in the eccentric training group, and 1.0 (SD 2.25) 4% of participants).Analysis 2.3 in the surgical group, a mean difference of -1.1 points (95% CI -2.2 to 0.1) or an absolute reduction, or worsening of, symptoms Harms of 10% (1% better to 22% worse). At 12 months, the mean global assessment of success was 3.0 (SD 1.6) in the eccentric training Neither study reported on adverse outcomes. group and 3.2 (SD 1.8) in the surgical group, a mean improvement Subgroup analysis and sensitivity analysis of 0.2 points (95% CI -0.8 to 1.7) or an absolute improvement of 2% (8% worse to 17% better). Based on low-certainty evidence Our planned subgroup analysis to assess if any differences in (one study, 40 participants), there was no clinically important outcome occurred with arthroscopic or open surgical excision difference between eccentric training and surgery in the proportion could not be performed as we did not identify more than one study of participants who rated treatment as successful at six or 12 with a common comparator. As we were unable to conduct a meta- months. Analysis 1.4 analysis, we did not perform any sensitivity analyses.

Return to sport D I S C U S S I O N

For return to sport, 6/20 (or 300 per 1000) in the eccentric group and Summary of main results 5/20 (or 250 per 1000) in the open surgical excision group returned to pre-injury participation levels with no pain: RR 0.83 (95% CI There is a limited number of randomised controlled trials assessing 0.30 to 2.29). This equates to an absolute risk difference of 5% less the benefit of surgical intervention for patellar tendinopathy. We success (33% less to 23% more) and a relative change of 17% less identified two studies, which were at risk of several biases. The success (70% fewer to 129% more) in the open surgical excision evidence underpinning the major outcomes was of low or very low group. Analysis 1.5 certainty, due to risk of bias in the trials and imprecision resulting from small sample sizes. 2. Arthroscopic surgery compared to sclerosing injections Low-certainty evidence from a single trial comparing open surgical Willberg 2011 compared arthroscopic surgery with sclerosing excision with eccentric exercises over 12 months (Bahr 2006) injections in 52 participants (26 in each group). Compared indicates that there may be no difference between interventions with sclerosing injection, low-certainty evidence (downgraded for at 12 months in terms of pain, functional outcomes or participant- imprecision, detection and reporting bias) shows that arthroscopic perceived benefit. surgery reduces pain and improves participant global assessment of success. Functional outcome scores were not reported, and Low-certainty evidence from a single trial comparing arthroscopic quality of life was not measured in the trial. The proportion of surgical debridement with sclerosing injections over 12 months participants with adverse events, and specifically the proportion (Willberg 2011) indicates possible greater improvements in pain with tendon rupture, was not reported. The minor outcome (return with activity, and higher participant satisfaction levels, with to sport) was also not reported. As there was no trial protocol we arthroscopic surgery. Functional outcome was not reported, cannot confirm if any of the outcomes not reported were measured. possibly due to selective reporting. See Summary of findings 2. Neither trial reported quality-of-life assessment or adverse events, Knee pain including tendon ruptures. Low-certainty evidence shows that, compared to sclerosing injections, surgery results in a clinically important reduction in Overall completeness and applicability of evidence pain (one study, 52 participants). At 12 months, mean pain during As we did not identify any placebo-controlled trials, we cannot draw activity on a 100-point scale (where a lower score indicates less any conclusions regarding the benefit of surgery. pain) was 41.1 (SD 28.5) in the sclerosing injection group and 12.8 (SD 19.3) in the arthroscopic surgery group. The absolute One study (Willberg 2011) reported an improvement in pain change was 28% better (15% to 42% better, the minimal clinically on activity with arthroscopic surgery compared to sclerosing important difference being 15%) and the relative change was 41% injections, not a placebo and therefore there is no standard better (21% to 61% better). No data were reported at six months, comparator in this trial. although outcomes were measured at this time point. Analysis 2.1 Patella tendinopathy is primarily a condition affecting athletes; the Participant global assessment of success authors of Willberg 2011 chose not to use a validated outcome At 12 months, the mean participant global assessment of success score, such as VISA score or Blazina grading, and did not report all on a 100-point scale (where a higher score indicates greater recorded time points. A lack of blinding was also evident. This bias,

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Willberg and colleagues reported on athletes who were non-elite Overall the quality of evidence can be considered low according the but had high activity levels, whilst Bahr and colleagues reported GRADE recommendations, which means the true effect might be on elite athletes; therefore the applicability of the evidence is markedly different from the estimated effect. limited to these patient populations. However, the condition is not normally seen in the non-athletic population. Potential biases in the review process

Eccentric exercises are currently considered the mainstay of We feel the lack of studies is a reflection of the paucity of the treatment for patella tendinopathy, although the benefits are research on the topic and is not necessarily due to publication bias, uncertain (Lopes 2018). In Bahr 2006, 25% of the participants as no ongoing studies were identified. showed no improvement with eccentric exercises and crossed Two review authors independently assessed the trials for inclusion, over to surgery during the study. This subset of participants had extracted data and assessed the risk of bias, and a third poorer outcome scores than the rest of the participants in the review author adjudicated whenever there was any discrepancy. trial. An intention-to-treat analysis accounted for this. However, the This approach minimises any biases in data extraction and rest of the participants' outcomes improved with time, and both management. groups were exposed to eccentric exercises, which could mean the eccentric exercises alone may have provided the treatment benefit. There is the potential for performance and detection bias in open studies when the main outcomes are self-reported. As we did not Despite a paucity of evidence, surgery is still utilised in clinical identify any trials comparing surgery with placebo (sham) we chose practice once all other mechanisms have been exhausted in the most common therapy, eccentric exercises, as our primary refractory cases. The two trials included in this review used comparator. different surgical techniques, targeting different areas of the presumed pathology. This highlights the lack of consensus on the Agreements and disagreements with other studies or pathophysiology of the injury and treatment. reviews Optimal treatments for patellar tendinopathy are still unknown, High rates of satisfaction and clinical improvement are reported however prospective studies suggest that athletes are more likely with case series publications that utilise retrospective data to be forced to retire with the condition if left untreated Kettunen( collection and subjective outcome measures, given the natural 2002). history of the condition (Ogon 2006).

Quality of the evidence A systematic review of all treatments for patellar tendinopathy has been performed (Larsson 2012). This was a systematic review We identified only two randomised controlled trials comparing exploring all treatment options, however it did not include Willberg surgery to non-operative interventions. Evidence for each outcome 2011 due to the search date (it only included Bahr 2006). The was downgraded at least twice, due to the potential for bias review concluded that there was a lack of evidence to support and imprecision. Studies were hampered by the potential for surgery and further research is needed (Larsson 2012). A review performance and detection bias (due to the difficulty in blinding of surgical interventions (Khan 2016) did identify both the trials participants and investigators to the intervention), attrition bias included in our review, but the authors only extracted data from (due to missing data), and use of non-validated outcome measures the surgically treated group, and did not compare the outcomes in one study (Willberg 2011), which resulted in potential reporting of surgery to non-surgical interventions. Khan 2016 concluded bias. Both trials failed to report adverse events, including tendon that surgery results in good success rates, but acknowledged that rupture, which also contributed to the high risk of reporting bias, higher-level evidence was needed. This is in accordance with the and meant we could not calculate any risk estimates for this events. findings of our review, which identified only two eligible trials and Data for each outcome came from single, small studies, which low-certainty evidence around the benefit of surgery. resulted in imprecision.

One study (Bahr 2006) compared surgical excision to eccentric A U T H O R S ' C O N C L U S I O N S exercises. Knee pain, functional outcome (VISA score), global Implications for practice assessment score and withdrawal rate were downgraded to low- certainty due to bias and imprecision. There was no inconsistency Due to the low certainty of evidence in this review, we are unable of effect as outcomes came from a single study, and no indirectness to draw conclusions about whether surgery is beneficial over other or publication bias. Quality-of-life measures, adverse events and non-operative measures for patellar tendinopathy. Surgery seems tendon rupture were not reported. to be considered in clinical practice for the late stages of patella tendinopathy due to exhaustion of other therapeutic methods Evidence comparing arthroscopic surgery to sclerosing injections rather than evidence of benefit. Given that no treatment results in also came from a single study (Willberg 2011). Knee pain and poor outcomes, we cannot support or refute the decision to operate global assessment score were downgraded to low-certainty due to when other less invasive and more evidence-based approaches imprecision and the risk of detection and performance bias. Due have failed. to very low event rates, we further downgraded the evidence on withdrawal rates to very low certainty. We did not downgrade for consistency of effect, indirectness or publication bias. Functional

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Implications for research Harms of surgery may be better addressed by reviewing prospective observational studies, preferably from surgery It is uncertain if open surgical excision offers more benefits than registries, given the apparent rare incidence of events such as eccentric exercises, as only low-certainty evidence was available tendon rupture. The incidence of infection in this population from a single trial with a high risk of biased results. Thus, larger is expected to be less than one per cent, and more serious well-designed trials are needed to determine if open surgery is complications (including tendon rupture) are reported very rarely, beneficial. One study (Willberg 2011) concluded that arthroscopic so it is not possible to estimate the comparative risks from the surgery is a superior treatment to sclerosing injections, however available randomised controlled trials. the evidence is of low certainty due to bias and imprecision. If arthroscopic surgery is thought to have a true effect on A C K N O W L E D G E M E N T S the outcome for patella tendinopathy, then further high-quality randomised controlled trials — with comparators of placebo and We would like to thank Helen Robinson from St Vincent's Hospital possibly eccentric exercises — are needed to establish efficacy of Library, Dublin, for her assistance with the literature search. arthroscopic surgery itself and potential superiority to the mainstay of non-operative treatment.

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REFERENCES

References to studies included in this review Additional references Bahr 2006 {published data only} Blazina 1973 Bahr R, Fossan B, Loken S, Engebretsen L. Surgical treatment Blazina ME, Kerlan RK, Jobe FW, Carter VS, Carlson GJ. Jumper's compared with eccentric training for patellar tendinopathy knee. Orthopedic Clinics of North America 1973;4(3):665-78. (Jumper's Knee). A randomized, controlled trial. Journal of Bone and Joint Surgery - American volume 2006;88(8):1689-98. Brockmeyer 2015 Brockmeyer M, Diehl N, Schmitt C, Kohn DM, Lorbach O. Willberg 2011 {published data only} Results of surgical treatment of chronic patellar tendinosis Willberg L, Sunding K, Forssblad M, Fahlstrom M, Alfredson H. (jumper’s knee): a systematic review of the literature. Journal of Sclerosing polidocanol injections or arthroscopic shaving to Arthroscopy 2015;31(12):2424-9. treat patellar tendinopathy/jumper's knee? A randomised controlled study. British Journal of Sports Medicine Cates 2008 [Computer program] 2011;45(5):411-5. Cates C. Visual Rx. Version 3. Dr Christopher Cates, 2008.

Cook 1997 References to studies excluded from this review Cook JL, Khan KM, Harcourt PR, Grant M, Young DA, Bonar SF. Coleman 2000 {published data only} A cross sectional study of 100 athletes with jumper’s knee managed conservatively and surgically. The Victorian Institute Coleman BD, Khan KM, Kiss ZS, Bartlett J, Young, DA, Wark, JD. of Sport Tendon Study Group. British Journal of Sports Medicine Open and arthroscopic patellar tenotomy for chronic patellar 1997;31:332-6. [DOI: http://dx.doi.org/10.1136/bjsm.31.4.332] tendinopathy. A retrospective outcome study. Victorian Institute of Sport Tendon Study Group. American Journal of Sports Cook 2001 Medicine 2000;28(2):183-90. Cook JL, Khan KM. What is the most appropriate treatment Cuellar 2007 {published data only} for patellar tendinopathy?. British Journal of Sports Medicine 2001;35(5):291-4. Cuellar EC, Mina NZ. Jumper's knee. Surgery and arthroscopic treatment with scraping and povidone collagen in Deeks 2017 high-performance athletes. Acta Ortopedica Mexicana Deeks JJ, Higgins JPT, Altman DG (editors). Chapter 9: 2007;21(5):234-8. Analysing data and undertaking meta-analyses. In: Higgins Dragoo 2011 {published data only} JPT, Churchill R, Chandler J, Cumpston MS (editors), Cochrane Handbook for Systematic Reviews of Interventions version Dragoo J, Wasterlain A. Double-blind randomized controlled 5.2.0 (updated June 2017). Cochrane, 2017. Available from trial of platelet-rich-plasma versus dry needling for treatment www.training.cochrane.org/handbook. of patellar tendinosis. Arthroscopy - Journal of Arthroscopic and Related Surgery 2011;1:e118-9. Ferretti 1985 Gaida 2011 {published data only} Ferretti A, Puddu G, Mariani PP, Neri M. The natural history of jumper's knee. Journal of International Orthopaedics Gaida JE, Cook J. Treatment options for patellar 1985;8(4):239-42. tendinopathy: critical review. Current Sports Medicine Reports 2011;10(5):255-70. Ferretti 1986 MarcheggianiMuccioli 2013 {published data only} Ferretti A. Epidemiology of jumper’s knee. Journal of Sports Medicine 1986;3(4):289–95. Marcheggiani Muccioli GM, Zaffagnini S, Tsapralis K, Alessandrini E, Bonanzinga T, Grassi A, et al. Open versus Figueroa 2016 arthroscopic surgical treatment of chronic proximal patellar Figueroa D, Figueroa F, Calvo R. Patellar tendinopathy: tendinopathy. A systematic review. Knee Surgery, Sports diagnosis and treatment. Journal of the American Academy of Traumatology, Arthroscopy 2013;21(2):351-7. Orthopaedic Surgeons 2016;24(12):e184-92. Sunding 2015 {published data only} GRADEpro GDT 2015 [Computer program] Sunding K, Willberg L, Werner S, Alfredson H, Forssblad M, McMaster University (developed by Evidence Prime, Inc.). Fahlstrom M. Sclerosing injections and ultrasound-guided GRADEpro GDT. Hamilton (ON): McMaster University (developed arthroscopic shaving for patellar tendinopathy: good clinical by Evidence Prime, Inc.), accessed prior to 4 May 2018. results and decreased tendon thickness after surgery — a medium-term follow-up study. Knee Surgery, Sports Hawker 2011 Traumatology, Arthroscopy 2015;23(8):2259-68. Hawker GA, Mian S, Kendzerska T, French M. Measures of adult pain: Visual Analog Scale for Pain (VAS Pain), Numeric Rating Scale for Pain (NRS Pain), McGill Pain Questionnaire (MPQ), Short-Form McGill Pain Questionnaire (SF-MPQ), Chronic Pain

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Grade Scale (CPGS), Short Form-36 Bodily Pain Scale (SF-36 JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch BPS), and Measure of Intermittent and Constant Osteoarthritis VA (editors), Cochrane Handbook for Systematic Reviews of Pain (ICOAP). Arthritis Care and Research 2011;63(11):240-52. Interventions. London: Cochrane.

Hernandez-Sanchez 2014 Lian 2005 Hernadez-Sanchez S, Hidalgo MD, Gomez A. Responsiveness Lian OB, Engebretsen L, Bahr R. Prevalence of jumper's knee of the VISA-P scale for patellar tendinopathy in athletes. British among elite athletes from different sports: a cross-sectional Journal of Sports Medicine 2014;48(6):453-7. study. American Journal of Sports Medicine 2005;33(4):561-7.

Higgins 2017 Lopes 2018 Higgins JPT, Altman DG, Sterne JAC (editors). Chapter 8: Lopes AD, Hespanhol Junior L, Kamper SJ, Costa LOP. Exercise Assessing risk of bias in included studies. In: Higgins JPT, for patellar tendinopathy. Cochrane Database of Systematic Churchill R, Chandler J, Cumpston MS (editors), Cochrane Reviews 2018, Issue 7. [DOI: 10.1002/14651858.CD013078] Handbook for Systematic Reviews of Interventions version 5.2.0 (updated June 2017). Cochrane, 2017. Available from Malliaras 2013 www.training.cochrane.org/handbook. Malliaras P, Barton CJ, Reeves ND, Langberg H. Achilles and patellar tendinopathy loading programmes: a systematic Kaeding 2006 review comparing clinical outcomes and identifying Kaeding CC, Pedroza AD, Powers BC. Surgical treatment of potential mechanisms for effectiveness.Sports Medicine chronic patellar tendinosis. Clinical Orthopaedics and Related 2013;43(4):267-86. Research 2006;455:102-6. Mourad 1988 Kettunen 2002 Mourad K, King J, Guggiana P. Computed tomography and Kettunen JA, Kvist M, Alanen E, Kujala UM. Long term prognosis ultrasound imaging of jumper's knee-patellar tendinitis. Journal for jumper's knee in male athletes: a prospective follow-up of Clinical Radiology 1988;39(2):162-5. study. American Journal of Sports Medicine 2002;30:689-92. Ogon 2006 Khan 1996 Ogon P, Maier D, Jaeger A, Suedkamp NP. Arthroscopic patella Khan KM, Bonar F, Desmond PM, Cook JL, Young DA, release for the treatment of chronic patellar tendinopathy. Visentini PJ, et al. Patellartendinosis (jumper’s knee): Arthroscopy 2006;22(4):462. findings at histopathologic examination, US, and MR imaging. Victorian Institute of Sport Tendon Study Group. PRISMA Group 2009 Radiology 1996;200:821-7. [DOI: http://dx.doi.org/10.1148/ Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group. radiology.200.3.8756939] Preferred Reporting Items for Systematic Reviews and Meta- Analyses: the PRISMA Statement. BMJ 2009;339:b2535. [DOI: Khan 1999 10.1136/bmj.b2535] Khan KM, Visentini PJ, Kiss ZS, Desmond PM, Coleman BD, Cook JL, et al. Correlation of ultrasound and magnetic RevMan 2014 [Computer program] resonance imaging with clinical outcomeafter patellar The Nordic Cochrane Centre, The Cochrane Collaboration. tenotomy: prospective and retrospective studies. Victorian Review Manager 5 (RevMan 5). Version 5.3. Copenhagen: The Institute of Sport Tendon Study Group. Clinical Journal of Sport Nordic Cochrane Centre, The Cochrane Collaboration, 2014. Medicine 1999;9(3):129-37. Roels 1978 Khan 2002 Roels J, Martens M, Mulier JC, Burssens A. Patellar tendinitis Khan KM, Cook JL, Kannus P, Maffulli N, Bonar SF. Time to (jumper's knee). American Journal of Sports Medicine abandon the 'tendinitis' myth. BMJ 2002;234(7338):626-7. 1978;6(6):362-8.

Khan 2016 Romeo 1999 Khan WS, Smart A. Outcome of surgery for chronic patellar Romeo AA, Larson RV. Arthroscopic treatment of infrapatellar tendinopathy: A systematic review. Acta Orthopædica Belgica tendonitis. Orthopedics and Sports Medicine 1999;15(3):341-5. 2016;82(3):610-26. Schünemann 2017a Larsson 2012 Schünemann HJ, Oxman AD, Higgins JPT, Vist GE, Glasziou P, Larsson M, Kall I, Nilsson-Helander K. Treatment of patellar Akl E, et al. the Cochrane GRADEing Methods Group and the tendinopathy- a systematic review of randomized controlled Cochrane Statistical Methods Group. Chapter 11: Completing trials. Knee Surgery, Sports Traumatology, Arthroscopy ‘Summary of findings’ tables and grading the confidence in or 2012;20(8):1632-46. quality of the evidence. In: Higgins JPT, Churchill R, Chandler J, Cumpston MS (editors), Cochrane Handbook for Systematic Li 2019 Reviews of Interventions version 5.2.0 (updated June 2017). Li T, Higgins JPT, Deeks JJ (editors). Chapter 5: Collecting Cochrane, 2017. Available from www.training.cochrane.org/ data. Draft version (29 Janurary 2019) for inclusion in: Higgins handbook.

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Schünemann 2017b Sterne 2017 Schünemann HJ, Oxman AD, Vist GE, Higgins JPT, Sterne JAC, Egger M, Moher D, Boutron I (editors). Chapter Deeks JJ, Glasziou P, et al. the Cochrane Applicability and 10: Addressing reporting biases. In: Higgins JPT, Churchill Recommendations Methods Group. Chapter 12: Interpreting R, Chandler J, Cumpston MS (editors), Cochrane Handbook results and drawing conclusions. In: Higgins JPT, Churchill for Systematic Reviews of Interventions version 5.2.0 R, Chandler J, Cumpston MS (editors), Cochrane Handbook (updated June 2017). Cochrane, 2017. Available from for Systematic Reviews of Interventions version 5.2.0 www.training.cochrane.org/handbook. (updated June 2017). Cochrane, 2017. Available from www.training.cochrane.org/handbook. Visentini 1998 Visentini P, Khan K, Cook J, Kiss Z, Harcourt P, Wark J. The VISA score: an index of severity of symptoms in patients with jumper's knee (patellar tendinosis). Journal of Science and Medicine in Sport 1998;1(1):22-8.

C H A R A C T E R I S T I C S O F S T U D I E S

Characteristics of included studies [ordered by study ID]

Bahr 2006 Methods Study design: randomised controlled trial, two groups

Study grouping: parallel group

Setting: participants were recruited from physicians and physical therapists referring participants to the Health Department at the Olympic Training Center in Oslo, Norway

Timing: March 2001 to September 2004 Intervention: open surgical excision combined with eccentric exercises versus physical therapy with eccentric exercises alone

Sample size: 15 participants required per group to have 90% power to detect a difference of mean dif- ference of 13 points on the Victorian Institute of Sport Assessment (VISA) score between groups in the primary endpoint; overall type-1 error rate was set at 5%

Analysis: intention-to-treat analysis planned and executed

Participants Number of participants

• 40 randomised (20 to eccentric training, 20 to open surgical excision) • At six-month follow-up there were 18/20 in the open surgical excision group and 20/20 in the eccentric exercise group included in the analysis. • At 12-month follow-up there were data for 20/20 (100%) for the open surgical excision group and 20/20 (100%) for eccentric exercise group.

Inclusion criteria

• History of exercise-related pain at the proximal part of the patellar tendon or the patellar insertion for at least three months, with Blazina scale (Lian modified) 3B symptoms - meaning the patient had to have pain during and after activity and had to be unable to participate in sports at the same level as before the onset of pain • Tenderness to palpation corresponding to the painful area • Magnetic Resonance Imaging (MRI) - thickening and increased signal intensity changes corresponding to the proximal part of the patellar tendon or the patellar insertion

Exclusion criteria

• History of knee or patellar tendon surgery • Had an inflammatory or degenerative joint condition • Less than 18 years old • Unable to understand oral and written Norwegian • Unwilling to undergo surgery (five participants)

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Bahr 2006 (Continued) Baseline characteristics: there was no demographic difference between groups. Listed recorded de- mographics include age, gender, height, weight, baseline VISA score, duration of symptoms, length of participation in sport and the amount or type of training.

Open surgical excision group

• Mean age: 30 (SD 8) years (3 female, 17 male) • Symptom duration: 35 (SD 30) months • Mean training hours: 12.2 (SD 7.3) • Mean pain score: 4.3 (SD 2.3) • Mean VISA functional score: 31 (SD 15)

Eccentric exercises group

• Mean age: 31 (SD 8) years (2 female, 18 male) • Symptom duration: 33 (SD 28) months • Mean training hours: 11.2 (SD 7.2) • Mean pain score: 3.9 (SD 2.7) • Mean VISA functional score: 29 (SD 16)

Interventions Open surgical excision

Surgery involved a 5 cm longitudinal midline incision from the inferior pole of the patella distally. A tourniquet was not used. The paratenon was split longitudinally and any pathologic paratenon tissue was removed. The tendon was split longitudinally in the midline to expose the deepest layers, and tis- sue that appeared abnormal was removed, or if not seen macroscopically the area calculated from the MRI was removed. Once the sutures were removed the participants were exposed to the same physio- therapist and eccentric exercises as the non-operative group. Two surgeons performed the operations.

Prior to starting the eccentric exercises participants gradually increased activities, focusing on knee range-of-motion and walking without crutches.

Eccentric exercise group

Involved use of a 25-degree decline board at home, where the downward (eccentric) component was performed on the affected leg and the upward (concentric) component was performed on the asymp- tomatic leg. The participant was instructed to perform the squat to 90 degrees with the back in a verti- cal position. The patient was instructed to take two seconds for the eccentric component. It involved twice-daily sessions of three sets of 15 repetitions for a total duration of 12 weeks, with weekly super- vision by a physiotherapist. No warm-up was performed. Six weeks after surgery, participants were ex- posed to the same rehabilitation/eccentric exercises programme as the eccentric exercise group, ex- cept they were not allowed to tolerate pain.

Both groups were allowed pain relief freely.

Outcomes Outcomes were assessed at baseline, 12 weeks, 6 months and 12 months by the trial authors. We report 6- and 12-month outcomes in this review.

Outcomes included in the trial

• Function: assessed by VISA zero-to-100 scale; 100 is full, pain-free function • Participant global assessment of treatment: measured on an 11-point numerical scale ranging from -5 (maximal deterioration in symptoms) to +5 (maximal improvement in symptoms) • Participant-reported overall treatment satisfaction, measured using four categories: no symptoms, improved, no change, or worse • Return to sport: measured using a four-point categorical scale, where 0 is no sport, 1 (reduced level), 2 (full training but some symptoms), 3 (full training and no symptoms). • Pain with jumping: assessed on 0- (no pain) to 10-point (maximum pain) visual analogue scale (VAS) for standing jumps and counter-movement jumps • Height of standing jumps and counter-movement jumps, in cm

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Bahr 2006 (Continued) • Strength: maximum load during leg extension using a leg press, in kg

Outcomes included in this review

• Pain: mean pain with standing jump on 0- to 10-point VAS • Function: mean score on zero-to-100 VISA scale • Participant global assessment: reported as proportion who reached full training and no symptoms • Proportion with adverse events

Identification Sponsorship source: one or more of the authors received grants or outside funding from Norwegian Eastern Health Corporate, Royal Norwegian Ministry of Culture, Norwegian Olympic Committee and Confederation of Sport, Norsk Tipping AS, and Pfizer AS.

Author's name: Roald Bahr

Institution: Norwegian School of Sport Sciences

Email: [email protected]

Address: Oslo Sports Trauma Research Center, Department of Sports Medicine, Norwegian School of Sport Sciences, P.O. Box 4014 Ullevaal Stadion, 0806 Oslo, Norway.

Notes Trial registration: none found

Data analysis: mean (95% confidence interval (CI)) function and participant global assessment of suc- cess at 6 and 12 months were extracted from the graph using PlotDigitizer (automeris.io/WebPlotDigi- tizer/).

Adverse events: one participant in the surgery group developed chronic quadriceps pain. Tendon rup- ture did not appear to be measured.

Withdrawals: none

Cross-overs: 5/20 in the eccentric exercise group had surgery.

Risk of bias

Bias Authors' judgement Support for judgement

Random sequence genera- Low risk "A randomisation sequence to surgical treatment or eccentric training (in tion (selection bias) blocks of four) was created by our statistician prior to the start of the study". It is likely this was adequate.

Allocation concealment Low risk "Sealed opaque envelopes used", and opened after a participant was enrolled (selection bias) in the study. This was probably sufficient to conceal treatment allocation.

Blinding of participants High risk Neither the participants or the investigators were blinded with regard to the and personnel (perfor- group allocation. There is potential for performance bias. mance bias) All outcomes

Blinding of outcome as- High risk Given that participants were allocated to surgery or exercises, blinding would sessment (detection bias) be difficult, thus there is a potential for detection bias in reporting pain, func- Self reported outcomes tion, and global evaluation.

Blinding of outcome as- Low risk This outcome was not measured in the study. sessment (detection bias) Assessor reported out- comes (tendon rupture)

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Bahr 2006 (Continued) Incomplete outcome data Low risk 5/20 participants from the eccentric exercises group crossed over to open sur- (attrition bias) gical excision, but final score before surgery was carried forward to 12 months All outcomes in the eccentric exercise group, which had the potential to attenuate any bene- fit of surgery if one existed. Post hoc analysis in the trial suggests no change in outcome over time with these participants.

Selective reporting (re- High risk Multiple outcomes reported. VISA score is the primary outcome and reported porting bias) as such. Pain was only reported at the 12-month time point. There is no proto- col publication and it is unclear if adverse events, including tendon rupture, were measured.

Other bias Low risk None apparent

Willberg 2011 Methods Study design: randomised controlled trial, two groups

Study grouping: parallel group

Setting: participants were recruited from Capio Artro Clinic in Stockholm, Sweden

Timing: not reported Intervention: sclerosing injection (polidocanol) versus arthroscopic surgery. Post intervention, both groups were allowed to weight bear as tolerated and increase loading as symptoms allowed from two weeks.

Sample size: 15 participants required per group to have 90% power to detect a difference of mean dif- ference of 13 points on the VISA score between groups in the primary endpoint; overall type-1 error rate was set at 5%

Analysis: intention-to-treat analysis

Participants Number of participants

• 52 participants were randomised (26 to sclerosing injection (Polidocanol) and 26 to arthroscopic surgery). • Data were available for 25 (96%) for the injection group and 25 (96%) for the arthroscopic surgery group at 12-month follow-up.

Inclusion criteria

• History and clinical examination consistent with proximal patella tendinopathy, long duration of symptoms, an athlete • Imaging-ultrasound showing the pathological changes in the thickened proximal patellar tendon were recorded

Exclusion criteria: acute presentation of pain

Baseline characteristics: there were no demographic differences.

Arthroscopic surgery group

• Mean age: 26.6 (SD 7.6) years (2 female, 24 male) • Symptom duration: 24 (SD 15.5) months • Mean training hours: not reported • Mean pain score: 76.5 (SD 13.6) • Mean VISA functional score: not reported

Sclerosing injection (Polidocanol) group

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Willberg 2011 (Continued) • Mean age: 27 (SD 7.6) years (2 female, 24 male) • Symptom duration: 20 (SD 10.4) months • Mean training hours: not reported • Mean pain score: 69 (SD 17.3) • Mean VISA functional score: not reported

Interventions Both interventions were performed under ultrasound and were doppler-guided.

Arthroscopic surgery

Arthroscopy was performed under local anaesthetic, using anterolateral and anteromedial portals. No tourniquet was used. The patella tendon insertion into the patella was identified following a rou- tine arthroscopic examination of the knee. A 4.5 mm shaver was utilised to destroy only the region with high blood flow and nerves adjacent to the tendinosis changes on the dorsal side of the tendon. No tendon tissue was resected and the Hoffa fat pad was saved. Portals were closed with tape. No informa- tion was given on who performed the surgeries.

Sclerosing injection (Polidocanol)

A 0.7 mm x 50 mm needle, connected to a 2 mL syringe, was utilised. Volumes of 0.1 mL to 0.2 mL were injected into the regions with local neovascularisation/high blood flow dorsal to the proximal patellar tendon. A maximum of three injections were given at six-week intervals. All injections were performed by the same, single sonographer.

Cointerventions

Both groups were allowed to weightbear fully post-treatment, and there was no specific rehabilitation protocol or preclusion of activities.

Outcomes Outcomes were assessed at baseline, 2 weeks, 3 weeks, 6 months and 12 months by the trial authors, but reported at only 12 months. We report outcomes at 12 months in this review.

Outcomes included in the trial

Pain - rest

• Pain at rest: mean pain assessed on a VAS of 0 mm (no pain) to 100 mm (maximal pain) • Pain during activity: mean pain assessed on a VAS of 0 mm (no pain) to 100 mm (maximal pain) with sporting activity • Participant-reported satisfaction with outcome: mean satisfaction assessed on a VAS of 0 mm to 100 mm (maximal satisfaction)

Outcomes included in this review

• Pain during activity: mean pain assessed on a VAS of 0 mm to 100 mm • Participant-reported satisfaction, mean satisfaction assessed on a VAS of 0 mm to 100 mm

Identification Sponsorship source: nil reported

Country: Sweden

Setting: Capio Artro Clinic, Stockholm

Author's name: Dr Lotta Willberg

Institution: Capio Artro Clinic, Stockholm

Email: [email protected]

Address: CapioArtro Clinic, StockholmSports Trauma Research Centre, Karolinska Institutet, Sophia- hemmet, Valhallavägen91, S-114 86 Stockholm, Sweden

Notes Trial registration: none found. Surgery for patellar tendinopathy (jumper’s knee) (Review) 27 Copyright © 2019 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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Willberg 2011 (Continued) Data analysis: mean (SD) pain and participant global assessment of success at 12 months was extract- ed from the study table.

Adverse events: no adverse events were reported.

Withdrawals: 1/26 participants withdrew in both groups.

Cross-overs: none

Risk of bias

Bias Authors' judgement Support for judgement

Random sequence genera- Unclear risk The method of sequence generation was not provided. tion (selection bias)

Allocation concealment Unclear risk Concealed envelopes were used, but participants selected their own envelope. (selection bias)

Blinding of participants High risk Study participants and investigators were not blinded and were aware of the and personnel (perfor- treatment; therefore there is a risk of performance bias. mance bias) All outcomes

Blinding of outcome as- High risk The participants were not blinded with regard to the group allocation. There sessment (detection bias) is potential for detection bias for self-reported outcomes (pain, function, glob- Self reported outcomes al evaluation) and performance-related outcomes (e.g. standing jump) due to knowledge of the allocated interventions by participants. The assistant col- lecting outcome scores was blinded to group allocation, however the data was recorded by participants who were not blinded, therefore there is a risk of de- tection bias.

Blinding of outcome as- Low risk Not relevant as none measured sessment (detection bias) Assessor reported out- comes (tendon rupture)

Incomplete outcome data Low risk 1/26 participants from both groups withdrew. (attrition bias) All outcomes

Selective reporting (re- High risk Complete data set not available for all mentioned time points. The study did porting bias) not report known outcome scores for patella tendinopathy (i.e. VISA) but may have recorded these.

Other bias Low risk None apparent

Characteristics of excluded studies [ordered by study ID]

Study Reason for exclusion

Coleman 2000 Not a randomised controlled trial

Cuellar 2007 Not a randomised controlled trial

Dragoo 2011 Not a surgical intervention

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Study Reason for exclusion

Gaida 2011 Not a randomised controlled trial (review article)

MarcheggianiMuccioli 2013 Not a randomised controlled trial (review article)

Sunding 2015 Not a randomised controlled trial

D A T A A N D A N A L Y S E S

Comparison 1. Open surgical excision vs eccentric exercises

Outcome or subgroup title No. of No. of Statistical method Effect size studies partici- pants

1 Knee Pain- standing jump 1 Mean Difference (IV, Fixed, 95% CI) Totals not selected

1.1 12 months 1 Mean Difference (IV, Fixed, 95% CI) 0.0 [0.0, 0.0]

2 Function (VISA) 0 to 100, 100 best 1 Mean Difference (IV, Random, 95% Totals not selected CI)

2.1 6 months 1 Mean Difference (IV, Random, 95% 0.0 [0.0, 0.0] CI)

2.2 12 months 1 Mean Difference (IV, Random, 95% 0.0 [0.0, 0.0] CI)

3 Global success - Proportion with no 1 Risk Ratio (M-H, Random, 95% CI) Totals not selected symptoms at 12 months

4 Global assessment of success 1 Mean Difference (IV, Fixed, 95% CI) Totals not selected

4.1 6 months 1 Mean Difference (IV, Fixed, 95% CI) 0.0 [0.0, 0.0]

4.2 12 months 1 Mean Difference (IV, Fixed, 95% CI) 0.0 [0.0, 0.0]

5 Return to sport 1 Risk Ratio (IV, Fixed, 95% CI) Totals not selected

5.1 12 months 1 Risk Ratio (IV, Fixed, 95% CI) 0.0 [0.0, 0.0]

Analysis 1.1. Comparison 1 Open surgical excision vs eccentric exercises, Outcome 1 Knee Pain- standing jump.

Study or subgroup Open surgical excision Eccentric exercises Mean Difference Mean Difference N Mean(SD) N Mean(SD) Fixed, 95% CI Fixed, 95% CI 1.1.1 12 months Bahr 2006 20 1.3 (0.8) 20 1.7 (1.6) -0.4[-1.18,0.38]

Open surgical excision -10 -5 0 5 10 Eccentric exercises

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Analysis 1.2. Comparison 1 Open surgical excision vs eccentric exercises, Outcome 2 Function (VISA) 0 to 100, 100 best.

Study or subgroup Open surgical excision Eccentric exercises Mean Difference Mean Difference N Mean(SD) N Mean(SD) Random, 95% CI Random, 95% CI 1.2.1 6 months Bahr 2006 18 58.9 (22.7) 20 55.7 (16.6) 3.24[-9.52,16]

1.2.2 12 months Bahr 2006 20 72.9 (11.7) 20 65.7 (23.8) 7.17[-4.45,18.79]

Eccentric exercises -100 -50 0 50 100 Open surgical excision

Analysis 1.3. Comparison 1 Open surgical excision vs eccentric exercises, Outcome 3 Global success - Proportion with no symptoms at 12 months.

Study or subgroup Open surgical excision Eccentric exercises Risk Ratio Risk Ratio n/N n/N M-H, Random, 95% CI M-H, Random, 95% CI Bahr 2006 5/20 7/20 0.71[0.27,1.88]

Eccentric exercises 1 Open surgical excision

Analysis 1.4. Comparison 1 Open surgical excision vs eccentric exercises, Outcome 4 Global assessment of success.

Study or subgroup Open surgical excision Eccentric exercises Mean Difference Mean Difference N Mean(SD) N Mean(SD) Fixed, 95% CI Fixed, 95% CI 1.4.1 6 months Bahr 2006 18 1 (2.3) 20 2 (1.3) -1.05[-2.24,0.14]

1.4.2 12 months Bahr 2006 20 3.2 (1.8) 20 3 (1.6) 0.21[-0.84,1.26]

Eccentric exercises -5 -2.5 0 2.5 5 Open surgical excision

Analysis 1.5. Comparison 1 Open surgical excision vs eccentric exercises, Outcome 5 Return to sport.

Study or subgroup Open surgical excision Eccentric exercises Risk Ratio Risk Ratio n/N n/N IV, Fixed, 95% CI IV, Fixed, 95% CI 1.5.1 12 months Bahr 2006 5/20 6/20 0.83[0.3,2.29]

Eccentric exercises 0.10.20.5 1 2 5 10 Open surgical excision

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Comparison 2. Surgery (arthroscopic) vs sclerosing injection

Outcome or subgroup title No. of No. of Statistical method Effect size studies partici- pants

1 Knee pain- functional VAS 1 Mean Difference (IV, Random, 95% CI) Totals not selected

1.1 12 months 1 Mean Difference (IV, Random, 95% CI) 0.0 [0.0, 0.0]

2 Global outcome of success- Satis- 1 Mean Difference (IV, Fixed, 95% CI) Totals not selected faction VAS

2.1 12 months 1 Mean Difference (IV, Fixed, 95% CI) 0.0 [0.0, 0.0]

3 Withdrawal rate 1 Odds Ratio (M-H, Fixed, 95% CI) Totals not selected

3.1 12 months 1 Odds Ratio (M-H, Fixed, 95% CI) 0.0 [0.0, 0.0]

Analysis 2.1. Comparison 2 Surgery (arthroscopic) vs sclerosing injection, Outcome 1 Knee pain- functional VAS.

Study or subgroup arthroscopic surgery sclerosing injection Mean Difference Mean Difference N Mean(SD) N Mean(SD) Random, 95% CI Random, 95% CI 2.1.1 12 months Willberg 2011 25 12.8 (19.3) 25 41.1 (28.5) -28.3[-41.79,-14.81]

arthroscopic surgery -100 -50 0 50 100 sclerosing injection

Analysis 2.2. Comparison 2 Surgery (arthroscopic) vs sclerosing injection, Outcome 2 Global outcome of success- Satisfaction VAS.

Study or subgroup arthroscopic surgery sclerosing injection Mean Difference Mean Difference N Mean(SD) N Mean(SD) Fixed, 95% CI Fixed, 95% CI 2.2.1 12 months Willberg 2011 25 86.8 (20.8) 25 52.9 (32.6) 33.9[18.74,49.06]

sclerosing injection -100 -50 0 50 100 arthroscopic surgery

Analysis 2.3. Comparison 2 Surgery (arthroscopic) vs sclerosing injection, Outcome 3 Withdrawal rate.

Study or subgroup arthroscopic surgery sclerosing injection Odds Ratio Odds Ratio n/N n/N M-H, Fixed, 95% CI M-H, Fixed, 95% CI 2.3.1 12 months Willberg 2011 1/26 1/26 1[0.06,16.89]

arthroscopic surgery 0.0020.1 1 10 500 sclerosing injection

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A P P E N D I C E S

Appendix 1. MEDLINE search strategy Database: Ovid MEDLINE

1. exp Tendon Injuries/ #21755

2. exp Tendinopathy/ #10946

3. tendin$.tw. #13145

4. tendon$.tw. #57876

5. (Tendon adj5 injur$).tw. #4146

6. or/1-5 #76738

7. exp Patellar Ligament/ #2163

8. patellar.tw. #11894

9. 7 or 8 #12268

10. 6 and 9 #5623

11. exp Arthroscopy/ #20930

12. exp Orthopedics/ #19441

13. patellar tenotomy.tw. #5

14. patellar release.tw. #15

15. patellar resection.tw. #31

16. or/11-15 #40099

17. 10 and 16 #652

18. randomized controlled trial.pt. #463482

19. controlled clinical trial.pt. #92483

20. randomized.ab. #405946

21. placebo.ab. #187154

22. drug therapy.fs. #2027759

23. randomly.ab. #287720

24. trial.ab. #422427

25. groups.ab. #1774877

26. or/18-25 #4183263

27 exp animals/ not humans.sh. #4470577

29 26 not 27 #3609587

30 17 and 29 #183

Appendix 2. CENTRAL search strategy Database: EBM Reviews - Cochrane Central Register of Controlled Trials (CCTR)

1. exp Tendon Injuries/ #635

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2. exp Tendinopathy/ #524

3. tendin$.tw. #981

4. tendon$.tw. #2627

5. (Tendon adj5 injur$).tw. #146

6. or/1-5 #3485

7. exp Patellar Ligament/ #126

8. patellar.tw. #968

9. 7 or 8 #984

10. 6 and 9 #554

11. exp Arthroscopy/ #1308

12. exp Orthopedics/ #323

13. patellar tenotomy.tw. #1

14. patellar release.tw. #4

15. patellar resection.tw. #3

16. or/11-15 #1620

17. 10 and 16 #66

Appendix 3. Embase search strategy Database: Ovid Embase

1. exp tendon injury/ #20600

2. exp tendinitis/ #12234

3. tendin$.tw. #16739

4. tendon$.tw. #69937

5. (Tendon adj5 injur$).tw. #4893

6. or/1-5 #94532

7. exp patellar ligament/ #881

8. patellar.tw. #14533

9. 7 or 8 #14698

10. 6 and 9 #6846

11. exp arthroscopy/ #27321

12. exp orthopedics/ #24716

13. patellar tenotomy.tw. #5

14. patellar release.tw. #20

15. patellar resection.tw. #31

16. or/11-15 #51720

17. 10 and 16 #660

Surgery for patellar tendinopathy (jumper’s knee) (Review) 33 Copyright © 2019 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

 Cochrane Trusted evidence. Informed decisions. Library Better health. Cochrane Database of Systematic Reviews

18. random$.tw. #1320273

19. factorial$.tw. #33239

20. crossover$.tw. #66795

21. cross over.tw. #29403

22. cross-over.tw. #29403

23. placebo$.tw. #277015

24. (doubl$ adj blind$).tw. #191199

25. (singl$ adj blind$).tw. #21424

26. assign$.tw. #342253

27. allocat$.tw. #129429

28. volunteer$.tw. #234838

29. crossover procedure/ #56154

30. double blind procedure/ #151893

31. randomized controlled trial/ #510308

32. single blind procedure/ #31885

33. or/18-32 #2034353

34. 17 and 34 #91

Appendix 4. Trial registries ClinicalTrials.gov (www.ClinicalTrials.gov) and the WHO trials portal (www.who.int/ictrp/en/) were searched using free-text terms, 'patella' and 'patellar tendinopathy' and found 21 registered trials; none were related to surgery.

H I S T O R Y

Protocol first published: Issue 5, 2018 Review first published: Issue 9, 2019

Date Event Description

6 May 2009 Amended CMSG ID: C186-P

14 November 2008 Amended Converted to new review format.

C O N T R I B U T I O N S O F A U T H O R S

Dr Michael Dan (MD) and Dr Alfred Phillips (AP) were responsible for writing and submitting the protocol, selecting studies and performing data extraction and analysis. Renea Johnston (RJ) contributed to double-checking risk of bias, assessing GRADE and writing and editing the review.

Professor Ian Harris (IH) is the supervising author who was responsible for overseeing and guiding MD and AP and contributing to writing, analysis and interpretation.

D E C L A R A T I O N S O F I N T E R E S T

Dr Michael Dan is undertaking a PhD into 'Patella tendinopathy and related ligamentous disorders'; he receives a Commonwealth (Australian Government) Research Training Program scholarship to subsidise his living costs to undertake his study.

Surgery for patellar tendinopathy (jumper’s knee) (Review) 34 Copyright © 2019 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

 Cochrane Trusted evidence. Informed decisions. Library Better health. Cochrane Database of Systematic Reviews

Renea Johnston is the Managing Editor of Cochrane Musculoskeletal, which is a recipient of a National Health and Medical Research Council Cochrane Collaboration Round 7 Funding Program Grant. The Program Grant supports the activities of Cochrane Musculoskeletal Australia but the funders have no role in the conduct or reporting of this or any Cochrane Reviews.

Professor Ian Harris and Dr Alfred Philips: none known.

S O U R C E S O F S U P P O R T

Internal sources • RTP Commonwealth scholarship, Australia.

Stipend for Dr Michael Dan to perform PhD at UNSW • University of New South Wales, Australia.

In kind support

External sources • No sources of support supplied

D I F F E R E N C E S B E T W E E N P R O T O C O L A N D R E V I E W

We planned to extract dichotomous measures of participant global assessment of success over continuous measures, if both were reported, as was the case in the study by Bahr 2006.

Willberg 2011 used the drug Polidocanol, which is the generic name. No trade name was utilised in the study methods description, therefore we did not search the relevant manufacturers' websites for trial information.

Main planned comparisons: we did not identify any studies that compared surgery to placebo.

If efficacy was established for surgery, we planned to compare open surgery versus arthroscopic surgery, but this could not be erformedp in this review.

Our planned subgroup analyses to assess if any differences in outcome occurred with arthroscopic or open surgical excision could not be performed as we did not identify more than one study with a common comparator.

Similarly, due to a paucity of studies, we could not perform planned sensitivity analyses.

I N D E X T E R M S

Medical Subject Headings (MeSH) *Patella; *Quality of Life; Arthroscopy [*methods]; Exercise Therapy; Pain Measurement; Randomized Controlled Trials as Topic; Tendinopathy [*surgery]; Treatment Outcome

MeSH check words Humans

Surgery for patellar tendinopathy (jumper’s knee) (Review) 35 Copyright © 2019 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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 The Knee 26 (2019) 1182–1191

Contents lists available at ScienceDirect

The Knee

The effect of surgery on patellar tendinopathy: Novel use of MRI questions the exploitability of the rat collagenase model to humans

Michael J. Dan ⁎, Rema A. Oliver, James D. Crowley, Vedran Lovric, William C.H. Parr, David Broe, Mervyn Cross, William R. Walsh

Surgical and Orthopaedic Research Laboratories (SORL), School of Clinical Sciences, Faculty of Medicine, University of New South Wales (UNSW), Level 1 Clinical Sciences Build- ing, Prince of Wales Hospital, Gate 6 Avoca Street, Randwick, New South Wales (NSW) 2031, Australia article info abstract

Article history: Background: patellar tendinopathy is an overuse condition most commonly affecting jumping Received 20 May 2019 athletes. Surgery is reserved for refractory cases; however, it lacks high level clinical evidence Received in revised form 20 October 2019 and basic science to support its use. The purpose of this study was to determine the biome- Accepted 22 October 2019 chanical and histological response of surgical excision on patellar tendinopathy in the rat col- Keywords: lagenase tendinopathy model and correlate MRI findings. Patellar tendinopathy Methods: Forty-eight Long Evans rats were divided into three groups: i) no patellar Collagenase tendinopathy with surgical excision, ii) patella tendinopathy with surgical excision, and iii) pa- Surgery tellar tendinopathy with no surgical excision. Endpoints included histology, mechanical testing, Animal model and MRI pre- and post-surgical intervention at one and four weeks. Rat Results: No difference in failure load or histological grading was seen between the groups at all time points. MRIs showed initial loss of tendon continuity followed by complete healing with elongated and thickened tendons in all groups. Conclusions: While other research has reported immunohistochemistry and histology of colla- genase-induced tendinopathy may be correlated with human pathogenesis, the novel MRI find- ings from our study suggest that the rat collagenase tendinopathy surgical model may be limited when extrapolating to humans. Further work is needed to determine if any correlation exists between the dosing, location, and animal effect of the collagenase injection model with MRI findings. This is needed before any collagenase model can be used to determine the effect of surgery in the pathogenic response to patella tendinopathy. © 2019 Elsevier B.V. All rights reserved.

1. Introduction

Patellar tendinopathy, an overuse condition affecting athletes, carries a poor prognosis with up to 53% of athletes retiring from sport due to the condition [1]. Physiotherapy, load management, and injectables are the main stay of treatment; however, 10% of patients require surgery. Traditionally, surgery involves excision of the diseased portion of the tendon (posterior superior tendon as it inserts onto the patella), with or without drilling the bone to stimulate new blood flow to promote healing [2,3]. The clinical effectiveness of surgery has been questioned by high level clinical evidence. Bahr et al. [4]foundnodifferencein patient outcomes between surgery and physiotherapy in a randomized control trial [4,5]. In comparison, lower level evidence of

⁎ Corresponding author at: Surgical & Orthopaedic Research Laboratories, Prince of Wales Hospital, Level 1, Clinical Sciences Building, Randwick, NSW 2031, Australia. E-mail address: [email protected]. (M.J. Dan).

https://doi.org/10.1016/j.knee.2019.10.017 0968-0160/© 2019 Elsevier B.V. All rights reserved.

Downloaded for Anonymous User (n/a) at Royal Australasian College of Surgeons from ClinicalKey.com.au by Elsevier on March 21, 2020.  For personal use only. No other uses without permission. Copyright ©2020. Elsevier Inc. All rights reserved. M.J. Dan et al. / The Knee 26 (2019) 1182–1191 1183 case series and case control studies have reported great benefittosurgery[6,7], in keeping with the view that the evidence to support surgery is indirectly proportional to the quality of the study [4]. The basic science supporting surgery is based on placing longitudinal incisions into the Achilles tendon of healthy rabbits that generated an increase in the macroscopic appearance of the tendon, believed to translate to increased tensile strength, leading to the rationale of replacing a ‘bad scar’ with a ‘good scar’ [8–10]. Animal models for tendinopathy have been created mechanically (through direct force) or chemically (by injection of collage- nase) while the direct correlation to the human pathological condition remains in question. The benefit to mechanically inducing tendinopathy is that it may more closely resemble the pathophysiology of tendinopathy in the human (repetitive overload). These models are limited in that the tendinopathy is not induced in the same location as humans and differences in kinematics are clearly different. Tendinopathy is induced in the mid substance of the tendon rather than the most common area in humans, which is the enthesis at the posterior superior patellar tendon [11–13]. The benefit of the chemical model induced through a col- lagenase injection is it allows for a reproducible dose-dependent response and is reported to be possible at an anatomical specific location similar to humans [14]. However, the reproducibility of this model remains in question. Reported results from rat tendinopathy models correlate well with known clinical data in some respects. There is good clinical data to support eccentric loading-based exercise therapy [15,16], along with good animal data to support tendon remodeling through mechano-transduction [17] even though the anatomical locations differ. However, in human patients, loading programs often do not show a benefit when performed during the sporting competition period [18], which correlates to detrimental effects of heavy loading too early after the development of patellar tendinopathy in animals [19]. The effect of surgery on patella tendinopathy at a histological and mechanical level has not been explored in humans or an- imals [17]. Given that collagenase rat tendinopathy models are often considered reflective of the human condition, this study aimed to investigate the histological and biomechanical effect of surgery on patellar tendinopathy in a rat model and correlate our findings with magnetic resonance imaging (MRI).

2. Methods

2.1. Animals

After approval of the Institutional Animal Care and Ethics Committee (ACEC approval 18/51A, UNSW, Australia), 48 female Long Evans rats (Biological Research Centre, Sydney, Australia), weighing on average 220 g, were equally divided and randomly assigned to three groups: i) no patellar tendinopathy with surgical excision, ii) patellar tendinopathy with surgical excision, and iii) patellar tendinopathy with no surgical excision. For those assigned to the tendinopathy group, collagenase was injected into the posterior superior patellar tendon bilaterally. Surgical excision was performed one week later. The same intervention and investigation were performed bilaterally in the same rat. Half the rats were then allocated for histological and MRI endpoints, whereas the other half were allocated solely for mechanical testing. Intervention and time points for each group were randomly allocated (Figure 1). Rats were acclimatized within their own groups with a maximum of four rats per cage, housed at 22 °C with 12-h day–night cycle, fed a standard laboratory diet of rat chow (Gordan's Specialty Stockfeeds, NSW, Australia) and water ad libitum. The rats were monitored daily each week post intervention and weighed weekly. Euthanasia was performed via carbon dioxide inhalation.

2.2. Anesthetic and perioperative care

Prior to collagenase injection and surgical excision, anesthesia was applied and maintained via isoflurane inhalation (two to three percent) with oxygen, titrated to effect. Rats were premedicated with buprenorphine 0.01 mg/kg s/c, 26-gauge insulin sy- ringe. Carprofen (two milligrams per kilogram s/c) was administered for post-operative analgesia and inflammation. Buprenorphine was administered for rescue analgesia as indicated. Rats were monitored daily for the first week following surgery, for pain, surgical wound irritation, appetite and behavioral changes.

2.3. Collagenase injection

For rats allocated to groups 2 and 3, at the initial time point T0 (Figure 1), a longitudinal 0.5 cm skin incision was performed directly over the patellar tendon under aseptic conditions. Type I collagenase (sigma 125CDU/mg) one milligram per milliliter dis- solved in 30 μl of phosphate-buffered saline (PBS) was injected into the posterior patella tendon using a 29-gauge insulin syringe. The needle was inserted along the length of the patella tendon from inferior portion until the inferior aspect of the patellar bone was felt, the collagenase was injected while slowly withdrawing to maximize placement in the posterior superior part of the pa- tellar tendon to replicate human location. Routine skin closure was performed using a buried cruciate suture using 4-0 braided multi-filament suture (Vicryl) (Figure 2a–d).

2.4. Surgical excision

For rats allocated to groups 1 and 2, at time point 1 (Figure 1), a longitudinal 1.5 cm skin incision was performed directly over the patellar tendon under aseptic conditions. A longitudinal incision was placed either side of the patellar tendon, medially and laterally, before placing the no. 15 blade through the tendon to excise the posterior and proximal 1/3. The procedure was

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Figure 1. Study flowchart. T0 = time zero when collagenase was injected to those groups allocated to collagenase injection — groups 2 and 3. T1 = one week post collagenase injection, when surgery was performed on those groups it was allocated to groups 1 and 2. Endpoints occurred both immediately before (T1 endpoint pre-surgery) and after surgery (T1 endpoint post-surgery). T2 = endpoint two weeks post collagenase injection (T0) and one week post-surgery (T1), T3 = end- point four weeks post-surgery (T1), five weeks post collagenase (T0). MT = mechanical testing, H = histology, MRI = magnetic resonance imaging. standardized regardless of the appearance of the patellar tendon on initial inspection (Figure 2e–g). Routine skin closure was then performed using a buried cruciate suture using 4-0 braided multi-filament suture (Vicryl) (Figure 2e–l).

2.5. Mechanical testing

Specimens allocated for mechanical testing were stripped of all soft tissue prior to testing. The tibia–patella tendon complex was mounted into custom-made jigs and tested using a Mach-1 testing system (Biosyntech Inc., Montreal, Quebec, Canada). The specimens were loaded to failure at a rate of 50 μm/s. Stiffness (linear portion of the load displacement curves) and maximum load to failure were calculated using Mach-1 analysis software. Testing was performed at room temperature and the sample kept hydrated with PBS. Fail- ure mode of the specimens was recorded as the site of the specimen failure: tendon mid substance, tibial enthesis, and patella enthesis.

2.6. Histology

Limbs were isolated and sectioned at the proximal femur and distal tibia knee joint. Specimens were fixed in 10% phosphate- buffered formalin for 48 h. Tissues were decalcified in 10% formic acid–formalin. The knee and patellar tendon complex were sec- tioned in the sagittal plane at the level of the cruciate ligaments and embedded in paraffin. Five-micrometer sections were cut

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Figure 2. a) Injection and surgical site: sterile preparation and draping. b) Longitudinal incision to directly visualize the patellar tendon–paratenon left intact. c) 29G needle inserted into the patellar tendon, from distal to proximal until the inferior edge of the patella bone was felt, the collagenase was then injected as slowly withdrawing. d) Buried cruciate stitch for meticulous closure. The macroscopic appearance of the patellar tendon at the time of surgical excision varied from e) normal white tendon, f) yellow discoloration, g) inflammatory mass to h) tendon rupture with femoral condyle on show. i–l) Regardless of the appearance, sur- gical excision was carried out by incising longitudinally medially and laterally on either side of the patellar tendon before placing the no. 15 blade across the ten- don to excise the posterior and proximal 1/3. using a Leica Microtome (Leica Microsystems, Germany) and stained using Harris hematoxylin and eosin. Histology was qualita- tively assessed for cellularity, vascularity, and collagen organization in a blinded fashion by two independent observers, quantified with a modified Movin score [20–22] as previously reported Orfei et al. [23](Table 1). Prior to formalin fixation, the limbs underwent examination with a 9.4-T MRI (Bruker BioSpin MRI GmbH) at the Mark Wain- wright Analytical Centre, UNSW. High resolution T2-weighted fast spin-echo images were acquired of the knee in the sagittal plane. Experimental parameters for these images included: slice thickness = 0.5 mm, spacing between slices = 0.5 mm, repeti- tion time [TR, ms] = 3300, echo time [TE, ms] = 26, number of averages = 6, imaging frequency = 400.34.

2.7. Statistical analysis

Statistical analysis for the quantitative parameters (mechanical testing and histology) between the groups was performed by Analysis of variance (ANOVA) post-hoc Tukey's Honest Significant Difference (HSD) test multiple comparison test to detect

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Table 1 Modified Movin Score. Grading system for the tendon histological evaluation.

01 2 3

Fiber structure and Normal: continuous, Slightly abnormal: partially Abnormal: moderately disorganized, Markedly abnormal: total disorganized arrangement parallel collagen fibers disorganized and fragmented fragmented, crossed and wavy fibers and non-identifiable fiber pattern fibers Cell density Normal Slightly increased Moderately increased Markedly increased Cell appearance Spindle-shaped cells Slightly rounded cells Moderately rounded cells Markedly rounded cells Inflammatory cell b10% 10–20% 20–30% N30% infiltration Neovascularization Normal presence of Slight increase of vascular bundles Moderate increase of vascular bundles Marked increase of vascular bundles vascular bundles Fatty deposits Absence of lipid Slight increase of lipid vacuoles Moderate increase of lipid vacuoles Marked increase of lipid vacuoles vacuoles

significant differences between the treatment groups. If the data was not normally distributed, non-parametric Kruskal–Wallis tests were used to compare the treatment effects. Significance was set to an alpha level of p b 0.05. All data are presented as the mean and the standard error of the mean. Intraclass correlation coefficients was used to determine the intra- and interob- server reliability for histology grading, with all samples reviewed by two independent graders and 22 random samples reviewed again by one grader. Analysis was performed using SPSS version 18.0 for Windows (SPSS Inc., Chicago, Illinois, USA).

3. Results

Direct vision was used to inject collagenase and provided a more accurate method than ultrasound guided administration due to the small nature of the rat patella tendon. All animals recovered well following the injection of collagenase or surgical intervention.

Figure 3. Ultimate load to failure. Ultimate load to failure (Newtons, SE) for each group reported as mean and standard error across time points (TP). Time point 0 = one week post tendinopathy, immediately post-surgical intervention, 1 = two weeks post tendinopathy, one week post-surgical intervention, 2 = five weeks post tendinopathy, four weeks post-surgical intervention.

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Figure 4. Stiffness. Stiffness (N/mm) for each group reported as mean and standard error across time points (TP). Time point 0 = one week post tendinopathy, immediate post-surgical intervention, 1 = two weeks post tendinopathy, one week post-surgical intervention, 2 = five weeks post tendinopathy, four weeks post- surgical intervention.

3.1. Mechanical testing

There was a mean difference between normal tendons and all the intervention groups (p b 0.01) at time 0 for ultimate load to failure. However, there was no difference between the intervention groups at all time points with a mean increase in the load to failure as the time points progressed (Figure 3). Intact normal tendons were stiffer (N/mm) when compared with all treatment groups studied, (p b 0.01). After one week, there was no difference in tendon stiffness between the groups following surgery. After four weeks post-surgery and five weeks following induction of tendinopathy, the no tendinopathy and surgery group (control) were significantly stiffer than both the tendinopathy groups (Figure 4; Table 2). The point of failure was significantly different between normal tendons, which failed at the inferior pole of the patella, 80% incidence, and mid substance, 20% incidence compared with treated groups, which failed at the mid substance, 90% incidence, (p b 0.01) at time point 0. There was no other statistically significant differences in failure point between groups across the time points.

3.2. Histology

The intraclass correlation coefficient for inter-observer reliability was 0.98, and 0.99 for intra-observer reliability. Following in- duction of tendinopathy, there was an increased number of round and inflammatory cells and loss of parallel orientation of col- lagen fibers with increased vascularity and fatty deposition with time (Figure 5). Similar changes were noted at the site of the surgical insult in the non-tendinopathy group. There was a substantial improvement with time. This improvement was reflected

Table 2 Mean and standard error for load to failure and stiffness at time points 1) immediately post-surgery, one and four weeks post-surgery.

No tendinopathy but surgery Tendinopathy and surgery Tendinopathy and no surgery

Time points Failure (N) Stiffness (N/mm) Failure (N) Stiffness (N/mm) Failure (N) Stiffness (N/mm)

Immediately post-surgery 15.82 (2.82) 1.32 (0.16) 16.70 (7.26) 0.97 (0.53) 11.08 (1.67) 0.53 (0.16) 1 week post-surgery 24.12 (3.17) 1.58 (0.16) 24.79 (2.78) 1.02 (0.11) 28.62 (4.97) 1.55 (0.21) 4 weeks post-surgery 43.83 (2.80) 2.57 (0.25) 50.81 (5.63) 1.55 (0.15) 44.05 (5.45) 1.61 (0.08)

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Figure 5. Normal vs tendinopathy tendon. Hematoxylin and eosin staining for normal tendon (top row) and one week post collagenase injection creating tendinopathy (bottom row) at 1.25× magnification, polarization, 4× and 10× magnification (left to right). Note the normal elongated spindle-shaped cells in the normal tendon, compared with the densely populated, disorganized (lack of polarization) plump fibroblastic cells with surround- ing lipid vacuoles and neovascularization in the tendinopathy subject. ☐ demonstrates area of higher magnification. 2020.

 M.J. Dan et al. / The Knee 26 (2019) 1182–1191 1189

Figure 6. Histology of treatment groups. Hematoxylin and eosin stain for surgical control, tendinopathy alone, and tendinopathy and surgery groups at 10× and 20× magnification. Both surgery and collagenase injection resulted in increased cell density, round plump fibroblastic cells, neovascularization, and lipid vacuoles. In all groups with time, the cell density decreased and the fibroblasts began to elongate. T0 = immediately post-surgical excision and one week post collagenase injection, T1 = one week post-surgical excision and two weeks post collagenase injection, and T2 = four weeks post-surgical excision and five weeks post colla- genase injection. by a decrease in round cells, decrease in the inflammatory response, and increasing numbers of spindle-shaped cells (Figure 6) with reorientation of collagen fibers seen on polarized light. Normal tendons scored a modified Movin score of 0/18. The surgery resulted in a score of 7.25 (SE 0.29), this was significantly different to both the tendinopathy groups (p = 0.02). At one week post tendinopathy injection, the mean score was 11.45 (SE 2.25) for the tendinopathy alone and 12.42 (SE 0.95) for tendinopathy and surgery, with no difference between tendinopathy groups (no surgery vs surgery) (p = 0.90). At one week post-surgery, two weeks post tendinopathy injection, there was no dif- ference between the groups. The mean score for the tendinopathy and surgery group was 15 (SE 0.71) compared with 13.25 (SE0.48) for the tendinopathy group (p = 0.55) and 11 (SE 1.78) for the surgical intervention alone group (p = 0.08). At four weeks post-surgery, five weeks post tendinopathy injection, there was no statistically significant difference between groups re- gardless of disease or treatment. This was reflected by a mean score for the tendinopathy and surgery group of 10.5 (SE 1.04), compared with 7.25 (SE 1.65) for the tendinopathy group (p = 0.26) and 9.25 (SE 1.31) for the surgical intervention alone group (p = 0.80).

3.3. MRI

Figure 7 demonstrates the variable tissue response to collagenase injection and surgical intervention. There was complete loss of the normal black tendon signal replaced with an enlarged high signal mass in its place. At the final time point, there was return of the normal black tendon signal; however, it was thickened and elongated compared with baseline.

4. Discussion

This study explored the basic science behind surgery for tendinopathy utilizing collagenase to simulate tendon pathology in a rat model with biomechanical testing, histology, and MRI. The overarching aim was to improve pathophysiology knowledge of the response to treatment, and thereby to improve treatment and clinical outcomes in patellar tendinopathy patients. We failed to show a difference in the histological response or the mechanical properties of the patellar tendon in rats with tendinopathy who underwent surgical excision compared with those that did not. We demonstrated that surgery alone results in a stiffer ten- don, which is weaker in the ultimate load to failure compared with the normal rat tendon. We did not detect any benefit follow- ing surgical excision of diseased patellar tendon from both a histological and mechanical strength viewpoint. This finding is in keeping with the lack of high level clinical evidence to support the use of surgical excision. Therefore, we cannot support the use of surgery for tendinopathy based on our findings [4]. The use of high resolution MRI, as reported in this study, points to dif- ferences in the rodent model that may limit its applicability to the human condition. Although high level clinical evidence is lacking [4,5], it is common practice for severe patellar tendinopathy patients to un- dergo surgical excision when non-operative management has been exhausted [2]. Animal tendinopathy models are utilized to in- vestigate the effect of treatment options on tendinopathy. While we failed to show a beneficial effect of surgery to the histological or mechanical strength of the tendinopathic tendon, the MRI findings of our study show that this model is not reflective of the condition in humans. The MRI findings in humans include ‘blurring’ of ligamentous margins and increased signal intensity within the patellar tendon on both short and long TE sequences [24,25]. All treatment groups demonstrated interruption of the

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Figure 7. T2-weighted sagittal MRI images of the rat knee at the level of the cruciate ligaments. Demonstrates injection and surgery contained to the patella ten- don. Increased signal intensity (* exemplifies this) at the area of the surgical excision (posterior to patella tendon) and collagenase injection. By the end of the study, all tendinopathy subjects healed with thickened and elongated patella tendons. T0 = immediately post-surgical excision and one week post collagenase injection, T1 = one week post-surgical excision and two weeks post collagenase injection, and T2 = four weeks post-surgical excision and five weeks post colla- genase injection. continuity of the patellar tendon, consistent with tendon rupture one week post collagenase injection. Five weeks post induction of tendinopathy, there was complete resolution of tendon integrity with the normal homogenous black tendon signal, regardless of surgical intervention; however, the tendon appeared thickened and elongated. The MRI findings documented following induction of tendinopathy is an important finding for the use of animal models, in particular for collagenase induced patellar tendinopathy. The rodent collagenase model is an accepted and reported model for the evaluation of patellar tendinopathy, while these models provide a reproducible animal model of patellar tendinopathy based on the immunohistological and histological response to the generation of tendinopathy akin to humans [11–13]. To the au- thors knowledge, there is only one other study that has utilized MRI imaging in a tendinopathy model. Following ultrasound- guided collagenase injection, Dominguez et al. [14] reported no loss of the characteristic black signal for healthy tendon or change in signal intensity within the tendon but with increased signal intensity within the knee joint and loss of cruciate ligament def- inition with 7T MRI. This, in conjunction with a lack of cellular change on histology suggests that the injection was given intra- articular and not intra-tendon, which we hypothesize is due to the technically challenging nature of ultrasound-guided injection into the rat patella tendon. During pilot procedures, experienced veterinary and orthopedic surgeons were unsuccessful in accu- rately and repeatedly injecting methyl blue dye within the tendon under ultrasound guidance. Therefore, we elected to administer the collagenase injection with direct supervision of the tendon, which we feel allows a more accurate delivery. Accuracy of our injection method is reflected in the consistency of histological findings with previously reported studies of tendon injury [23] and containment of MRI changes to the tendon itself rather than the knee joint. Our mechanical data indicates that the collage- nase preferentially concentrated its effect within the intrasubstance of the tendon rather than at the patellar tendon–bone enthesis, which our study aimed to reproduce like in humans. Our study demonstrates that while biochemically and histologically, collagenase models are reflective of human tendinopathy [11–13], the MRI appearance is more reflective of tendon rupture and not attune to what is seen in humans; increased signal intensity within the tendon [24]. This may limit the application of the ro- dent model for future studies. Our MRI results revealed a complete tendon rupture, which could reflect the dose and concentration of collagenase injection. However, our dose regimen was at the lower end of the reported reference range to induce tendinopathy, with similar modified Movin scores to those reported in the literature [23,26]. Our results support that while the histological and immunohistochemistry may be similar between collagenase models and human tendinopathy [11–13], there is a need to correlate these changes to the MRI findings in order to improve the applicability of animal models to the human condition. Therefore, it is reasonable to question the validity of treatment options for patella tendinopathy derived from animal models [26–30]. More investigation is needed to qualify and quantify the relationship between immunohistochemistry, histology, and MRI of different collagenase models for

Downloaded for Anonymous User (n/a) at Royal Australasian College of Surgeons from ClinicalKey.com.au by Elsevier on March 21, 2020.  For personal use only. No other uses without permission. Copyright ©2020. Elsevier Inc. All rights reserved. M.J. Dan et al. / The Knee 26 (2019) 1182–1191 1191 different animals to improve the applicability of these models to the human condition before any future preclinical treatment op- tions can be considered of any merit to apply to humans. The timing of surgical intervention seven days after collagenase was chosen to reflect a median tissue response during the acute injury phase between three and 15 days reported in the literature. The endpoint of one week post-surgery and four weeks post-surgery was designed to examine the acute and chronic surgical response given complete spontaneous resolution oc- curs by day 45 after injection without treatment [19,23]. A limitation of our study was the reduced numbers in each group per time point to allow for examination of histology and mechanical strength across the study period. However, given the potential limitations of the collagenase model based on our novel MRI investigation, an increase in numbers, based on the reduction and refinement principle [31], may not be warranted until issues with the applicability of the collagenase model have been addressed with further studies correlating the histology findings with MRI. Until animal tendinopathy models have been refined utilizing MRI to show better applicability to humans, its utility as a research tool is limited.

5. Conclusion

In conclusion, we found no difference in the healing response based on mechanical and histological findings to support surgi- cal excision for patellar tendinopathy. While immunohistochemistry and histology may be correlated with human pathogenesis, the 9.4 T MRI findings from our study suggest that applicability of the rat collagenase tendinopathy model to humans is question- able. It is important for the clinician to be aware of the limitations of any animal model when examining research exploring novel treatment options before applying to humans. Further investigation is needed to determine the relationship of MRI changes in animal-based tendinopathy models to facilitate thorough examination of the basic science effect of surgery, and other treatment modalities, for patellar tendinopathy and allow for applicability to humans.

Declaration of competing interest

None.

References

[1] Kettunen JA, et al. Long-term prognosis for Jumper's knee in male athletes: prospective follow-up study. Am J Sports Med 2002;30(5):689–92. [2] Figueroa D, Figueroa F, Calvo R. Patellar tendinopathy: diagnosis and treatment. J Am Acad Orthop Surg 2016;24(12):e184–92. [3] Maffulli N, Longo UG, Denaro V. Novel approaches for the management of tendinopathy. JBJS 2010;92(15):2604–13. [4] Bahr R, et al. Surgical treatment compared with eccentric training for patellar tendinopathy (Jumper's knee). A randomized, controlled trial. TJBJS 2006;88(8): 1689–98. [5] Dan M, Phillips A, Johnston RV, Harris IA. Surgery for patellar tendinopathy (Jumper's knee). Cochrane Database Syst Rev 2019(9). [6] Brockmeyer M, et al. Results of surgical treatment of chronic patellar tendinosis (Jumper's knee): a systematic review of the literature. Arthroscopy 2015;31(12) p. 2424–9.e3. [7] Coleman BD, et al. Studies of surgical outcome after patellar tendinopathy: clinical significance of methodological deficiencies and guidelines for future studies. Victorian Institute of Sport Tendon Study Group. Scand J Med Sci Sports 2000;10(1):2–11. [8] Leadbetter WB, et al. The surgical treatment of tendinitis. Clinical rationale and biologic basis. Clin Sports Med 1992;11(4):679–712. [9] Sharma P, Maffulli N. Tendon injury and tendinopathy: healing and repair. JBJS 2005;87(1):187–202. [10] Kader D, et al. Achilles tendinopathy: some aspects of basic science and clinical management. Br J Sports Med 2002;36(4):239–49. [11] Lake SP, Ansorge HL, Soslowsky LJ. Animal models of tendinopathy. Disabil Rehabil 2008;30(20–22):1530–41. [12] Hast MW, Zuskov A, Soslowsky LJ. The role of animal models in tendon research. BONE JOINT RES 2014;3(6):193–202. [13] Dirks RC, Warden SJ. Models for the study of tendinopathy. J Musculoskelet Neuronal Interact 2011;11(2):141–9. [14] Dominguez D, et al. Generation of a new model of patellar tendinopathy in rats which mimics the human sports pathology: a pilot study. Apunts-Med Esport 2017;52(194):53–9. [15] Young MA, et al. Eccentric decline squat protocol offers superior results at 12 months compared with traditional eccentric protocol for patellar tendinopathy in volleyball players. Br J Sports Med 2005;39(2):102–5. [16] Alfredson H, et al. Heavy-load eccentric calf muscle training for the treatment of chronic Achilles tendinosis. Am J Sports Med 1998;26(3):360–6. [17] Kaux J-F, et al. Eccentric training improves tendon biomechanical properties: a rat model. J Orthop Res 2013;31(1):119–24. [18] Visnes H, et al. No effect of eccentric training on Jumper's knee in volleyball players during the competitive season: a randomized clinical trial. Clin J Sport Med 2005;15(4):227–34. [19] Godbout C, Ang O, Frenette J. Early voluntary exercise does not promote healing in a rat model of Achilles tendon injury. J Appl Physiol 2006;101(6):1720–6. [20] Maffulli N, et al. Movin and Bonar scores assess the same characteristics of tendon histology. Clin Orthop Relat Res 2008;466(7):1605–11. [21] Movin T, et al. Tendon pathology in long-standing achillodynia. Biopsy findings in 40 patients. Acta Orthop 1997;68(2):170–5. [22] Maffulli N, et al. Similar histopathological picture in males with Achilles and patellar tendinopathy. Med Sci Sports Exerc 2004;36(9):1470–5. [23] Orfei CP, et al. Dose-related and time-dependent development of collagenase-induced tendinopathy in rats. PloS one 2016;11(8):e0161590. [24] Johnson DP, Wakeley CJ, Watt I. Magnetic resonance imaging of patellar tendonitis. Bone Joint J 1996;78(3):452–7. [25] Shalabi A, et al. MR evaluation of chronic Achilles tendinosis: a longitudinal study of 15 patients preoperatively and two years postoperatively. Acta Radiol 2001; 42(3):269–76. [26] Marcos RL, et al. Low-level laser therapy in collagenase-induced Achilles tendinitis in rats: analyses of biochemical and biomechanical aspects. J Orthop Res 2012; 30(12):1945–51. [27] Machova Urdzikova L, et al. Human multipotent mesenchymal stem cells improve healing after collagenase tendon injury in the rat. Biomed Eng Online 2014;13:42. [28] Casalechi HL, et al. Low-level laser therapy in experimental model of collagenase-induced tendinitis in rats: effects in acute and chronic inflammatory phases. Lasers Med Sci 2013;28(3):989–95. [29] Yoo SD, et al. Effects of extracorporeal shockwave therapy on nanostructural and biomechanical responses in the collagenase-induced Achilles tendinitis animal model. Lasers Med Sci 2012;27(6):1195–204. [30] Chen L, et al. Tendon derived stem cells promote platelet-rich plasma healing in collagenase-induced rat achilles tendinopathy. Cell Physiol Biochem 2014;34(6): 2153–68. [31] Grundy D. Principles and standards for reporting animal experiments in the journal of physiology and experimental physiology. J Physiol 2015;593(12):2547–9.

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 Original Research

Evaluation of Intrinsic Biomechanical Risk Factors in Patellar Tendinopathy

A Retrospective Radiographic Case-Control Series

Michael J. Dan,*† MBBS, MSc(Res), James McMahon,‡ MBBS, William C.H. Parr,† PhD, David Broe,† MBBCh, BAO, FRACS(Ortho), Phil Lucas,§ MBBS, FRANZCR, Meryvn Cross,|| MBBS FRACS(Ortho), OAM, and William R. Walsh,† PhD Investigation performed at the Surgical and Orthopaedic Research Laboratories, Prince of Wales Clinical School, University of New South Wales, Prince of Wales Hospital, Sydney, Australia

Background: Patellar tendinopathy is an overuse condition often affecting athletes. It has been postulated that patellar tendi- nopathy is associated with patella alta; however, this and any other anatomic risk factors have not been identified. Purpose: To explore whether lever arm differences from radiographic measurements exist between patients with and without tendinopathy. This may provide surgeons with a simple radiographic means to identify patients at risk. Study Design: Cross-sectional study; Level of evidence, 3. Methods: Magnetic resonance imaging scans of the knee from a sports imaging facility were screened and reviewed to identify 2 groups of patients: those with and those without imaging signs of patellar tendinopathy. The lateral radiographs were reviewed and measurements made to determine (1) lever arm ratio, (2) moment arm ratio, (3) angle between the moment and line of pull of the patellar tendon, (4) patellar tendon pivot point angle, and (5) patellar height (alta). Measurements were obtained directly from radiographs. The images and measurements were reviewed by 2 experienced orthopaedic clinicians. Results: A total of 105 patients were included in this study: 52 with patellar tendinopathy and 53 without patellar tendino- pathy (controls). The mean age was similar between groups (23 years); females accounted for 8 of 52 patients with patellar tendinopathy and 24 of 53 patients without. The lever arm ratio in the group with patellar tendinopathy versus controls was 1.71 versus 1.01 (P ¼ .01), with a moment arm difference of 1.00 versus 0.80 (P < .01), respectively. There was no difference detected between groups for patellar tendon angle, patellar tendon pivot point angle, knee flexion angle, or incidence of patella alta. No correlation was found with our measurements and the Insall-Salvati ratio. Statistical analysis was also performed according to sex, and a statistically significant difference between groups was found for differences in lever arm ratio and moment arm. Conclusion: The lever arm ratio and moment arm ratio from lateral radiographs were significantly different between patients with and without patellar tendinopathy. Further study is needed on the biomechanical implications of the pivot point and how altering it can affect stress within the patellar tendon, patellofemoral joint, and associated clinical outcomes. Keywords: jumper’s knee; tendinosis; biomechanics; knee; radiography

Patellar tendinopathy is an overuse condition commonly training volume and harder training surfaces have been affecting jumping athletes, with a reported incidence associated with development of this condition.6,18,22 >50% for volleyball and basketball players, as opposed to Intrinsic risk factors are those internal to the athlete/ an incidence of 20% among soccer players.14 Patellar tendi- patient. Patellar tendinopathy is more common among nopathy is characterized by anterior knee pain, with ten- patients with tight quadriceps and hamstring muscles,23 derness at the distal pole of the patella.4 The major risk abnormal leg lengths, and pes planus.18 Previous stud- factors for the condition are those that are extrinsic (ie, ies have failed to show a statistical difference in the external to the athlete/patient). In particular, increased morphology of the patella between those with and those without patellar tendinopathy.6,7,15 These studies exam- The Orthopaedic Journal of Sports Medicine, 6(12), 2325967118816038 ined the patella for differences in anatomy based on DOI: 10.1177/2325967118816038 radiographic risk factors associated with patellofemoral ª The Author(s) 2018 pain and dislocation.

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2 Dan et al The Orthopaedic Journal of Sports Medicine

Tyler et al17 successfully demonstrated differences in METHODS sagittal patellar tilt and described a new measurement for a patellofemoral relationship, called anteroposterior patel- Study Design lar tilt—specifically, the angle formed between the patel- lar articular surface and the anterior diaphyseal axis of A retrospective case-control series study of lateral planar the femur on lateral knee radiograph. In that study, radiographs was performed following ethical approval. patients with patellar tendinopathy had a mean of 4.5 The sample size was set at 50 per group: patients with less anteroposterior tilt compared with control partici- patellar tendinopathy and asymptomatic controls. We pants. These authors did not associate a clinical signifi- used a computer algorithm to screen the radiologist’s mag- cance to this as being either diagnostic or therapeutic, nor netic resonance imaging (MRI) report for appropriate did they provide a biomechanical explanation for why this patients. To screen for control patients, the algorithm difference existed. searched for the text “normal MRI” within the report. To As identified by Huberti et al,9 the patella should be screen for patients with patellar tendinopathy, the algo- viewed as a lever, not a pulley, with the patellar tendon: rithm searched for the terms “patella/r tendinopathy” and quadriceps force ratio changing according to the degree of synonyms “tendinosis” and “tendinitis.” Patient clinical knee flexion. The patellar tendon experiences relatively notes were not reviewed in this study, but the indication higher degrees of stress for the first 45 of flexion, before for MRI (as documented on the MRI referral) included the relationship is reversed to have a higher degree of quad- “anterior knee pain.” riceps stress relative to the patellar tendon.9 Van Eijden The MRI report and images from patients with tendino- and coauthors19-21 expanded on this, producing a series of pathywerereviewedtoconfirmthediagnosis.Thiswas mathematical equations to describe the position and force done by identifying thickening of the patellar tendon and increased signal intensity on both short and long echo time relationships of the patella in the sagittal plane. 11 The debate continues over the etiology of patellar tendi- MRI sequences in the tendinopathy cases. The next step nopathy as a stress-shielding/compressive phenomenon1,2 for inclusion was to ensure that all patients (control and versus a repetitive micro-overload pathogenesis. There is tendinopathy groups) had a recent lateral knee radiograph sufficient clinical evidence, however, to exclude compres- with MRI. Exclusion criteria included evidence of previous sive etiology16 and ample biomechanical cadaveric evidence surgery, knee effusion, quadriceps tendinopathy, or other and finite element models to support repetitive micro- intra-articular pathology that may have affected patellar overload,3,8,12 in keeping with the known overload extrinsic position or the indication for the original referral of inves- risk factors from clinical studies6,18,22 to support the etiology tigative imaging. We also excluded patients if they were < > of repetitive micro-overload. 16 years old, to ensure skeletal maturity, or 35 years We previously explored this topic in greater detail in an old, as a quasi-restrictor intended to minimize age-related extensive review of the literature on patellar tendinopa- tendinopathic changes. We did not match further for sex or thy and the biomechanics of the extensor mechanism.5 age to minimize selection bias. Considering the etiology of repetitive micro-overload, we hypothesized that the answer to identifying potential Measurements intrinsic risk factors lies in viewing the patella in the lat- eral plane as a lever in which, to be in equilibrium, the Radiographic measurements were performed on de- moments on either side must balance. The current study identified and scaled JPEGs of lateral knee radiographs. defines new lateral knee radiographic measurements with We used software written in Mathematica (v 10.1; Wolfram the aim of identifying intrinsic risk factors for patellar Language). The software allowed the examiners to place tendinopathy based on biomechanical principles obtained markings representing the points identified in Figures 1 from lateral radiographs. We analyzed differences in to 3 before the program would calculate the measurements patella-related lever measurements acquired through lat- described for each image. The radiographs were indepen- eral planar radiographs of patients with and without dently reviewed and marked by 2 blinded examiners to cal- patellar tendinopathy. culate the described measurements.

*Address correspondence to Michael J. Dan, MBBS, MSc(Res), Surgical and Orthopaedic Research Laboratories, Prince of Wales Clinical School, University of New South Wales, Prince of Wales Hospital, Barker Street, Sydney, NSW 2031, Australia (email: [email protected]). †Surgical and Orthopaedic Research Laboratories, Prince of Wales Clinical School, University of New South Wales, Prince of Wales Hospital, Sydney, Australia. ‡Orthopaedic Department, Royal Prince Alfred Hospital, Sydney, Australia. §PRP Diagnostic Imaging, Sydney, Australia. ||The Stadium Sports Medicine Clinic, Sydney, Australia. One or more of the authors has declared the following potential conflict of interest or source of funding: M.D. receives financial support in the form ofa Research Training Program stipend scholarship from the Australian government to complete his PhD. AOSSM checks author disclosures against the Open Payments Database (OPD). AOSSM has not conducted an independent investigation on the OPD and disclaims any liability or responsibility relating thereto. Ethical approval for this study was obtained from the Human Research and Ethics Committee of the University of New South Wales, Sydney, Australia (HC180197).

The Orthopaedic Journal of Sports Medicine Biomechanics in Patellar Tendinopathy 3

Figure 2. Moment arm ratio. Quadriceps tendon vector (QTV) and patellar tendon vector (PTV) are formed from a line continued with the soft tissue outline of the respective tendons. The moment arm (MA) is the perpen- dicular distance from the tendon vector to the pivot point (see Figure 1A for a description of the pivot point). The moment arm ratio is the MAQT divided by MAPT.F,femur; T, tibia.

Figure 1. Lever arm ratio. (A) Locating the pivot point: this is equivalent to the midpoint of the articulation of the patella on the femur. It is found by drawing 2 lines (labeled x) perpendicular to the patellar articular surface equidistant from the femoral articular surface proximally Figure 3. Angles and patellar height. Patellar height is and distally. The midpoint of these 2 points on the patellar defined by patellar tendon length (AB) divided by patellar articular surface is what we term the pivot point, equivalent length (BC). Knee flexion angle (Y)isformedbytheinter- to the fulcrum of the lever. (B) Lever: the lever is a line section of lines drawn parallel with the anterior part of the drawn from the quadriceps tendon insertion (QTI) to the posterior diaphyseal cortex of the femur and tibia.13 The patellar tendon origin/insertion (PTI). (C) Lever arm ratio: patellar tendon angle (b)isformedbytheanglebetween a line perpendicular to the patellar articular surface is AB and a line drawn perpendicular to BC at point B.The drawn from the pivot point to the lever. This divides the patellar tendon pivot point angle (a)isformedbythepatel- lever into the lever arms of the patellar tendon (LAPT)and lar tendon (AB) and a line drawn from B to the pivot point. quadriceps tendon (LAQT). The lever arm ratio is LAQT For an explanation of pivot point, see Figure 1A. F, femur; divided by LAPT.F,femur;P,patella;T,tibia. T, tibia.

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TABLE 1 intra- and interobserver reliability. The interobserver reli- Inter- and Intraobserver Reliability ability of the patellar tendon angle, with an ICC of 0.92, was Correlation Coefficientsa the lowest, whereas the knee flexion angle had the highest ICC, at 0.99. The patellar tendon angle had the lowest Measurement Interobserver Intraobserver intraobserver reliability, with an ICC of 0.90, and the knee Arm ratio flexion angle and lever arm ratio had the highest, at 0.99. Lever 0.97 0.99 Moment 0.96 0.92 Analysis Tendon angle Patella 0.92 0.90 Demographic data (Table 2) revealed a significantly higher Pivot point patella 0.95 0.95 number of females in the control group versus the tendino- Knee flexion angle 0.99 0.99 pathy group (P < .01). No differences were found with Alta 0.97 0.92 respect to age between groups. a A statistically significant difference was found in the A strong correlation was seen within the same observer and P ¼ P < between observers, reported as intraclass correlation coefficients. lever arm ratio ( .01) and the moment arm ratio ( .01) between patients with and without patellar tendinopa- thy. The tendinopathy group had mean lever and moment Measurement Points arm ratios of 1.71 and 1.00, respectively, as opposed to 1.01 and 0.80 for the control patients (Table 2). The relationship Our novel radiographic measurements apply lever princi- between values are further demonstrated in box plots in ples to the lateral knee radiograph, viewing the patella as a Figures 4 and 5 to present the spread of the data. Results lever, with the articulation point on the femur determining presented in Table 2 include the outliers listed in Figures 4 the fulcrum, as outlined in Figures 1 to 3. Torque is defined and 5. The results of the analysis were unchanged when by the force times the perpendicular distance from the axis these 5 outliers were removed. of rotation (lever arm) multiplied by the perpendicular com- Patellar tendon angle, patellar tendon pivot point angle, ponent of the force vector. Figure 1 describes how to iden- and the prevalence of patella alta were not statistically tify the pivot point/fulcrum and calculate the patellar different between controls and patients with patellar ten- tendon and quadriceps tendon lever arms. Figure 2 dinopathy. Knee flexion angle was also not statistically dif- describes how to calculate the moment arms of the patellar ferent. Data were analyzed with respect to sex, and tendon and the quadriceps tendon. The effect of the angle of statistically significant between-group differences in the pull from the vector of the patellar tendon is determined lever arm ratio and moment arm ratio were still of compa- by calculating the patellar tendon angle as described in rable magnitude (Table 2). No other statistically significant Figure 3. The pivot point patellar tendon angle investigates differences were found in the sex analysis. the combined effect of the lever arm length with the patel- It is known that the articulation point of the patella changes lar tendon angle. This and the patellar tendon height from the distal pole in extension to the proximal pole in flexion; AB BC (Insall-Salvati method: patella alta was defined as / however, the scatter plot shown in Figure 6 failed to demon- > 10 1.2) are also described in Figure 3. strate this linear relationship between knee flexion angle and lever arm ratio across patients in our study. There was no Statistical Analysis difference in the knee flexion angle between the control and patellar tendinopathy groups (Table 2). We performed a sub- Interobserver reliability was compared for all radiographic analysis of the controls and patellar tendinopathy patients measurements described in Figures 1 to 3. Twenty radio- using knee flexion angles of 30 to 60 and 60 to 80 . There graphs were randomly selected to be remeasured by the wasanevenspreadofpatientsineachgroup,withmeandif- first observer to test intraobserver reliability. Reliability ferences of 0.43 and 0.62 for the lever arm (P ¼ .01) and 0.23 was tested with the intraclass correlation coefficient (ICC) and 0.21 for the moment arm (P ¼ .04), respectively. The via a 2-way mixed model. A 2-tailed Student t test for inde- remaining variables were still not statistically significant. pendent samples was used to compare means between the There was no statistically significant correlation of the lever controls and the patients with patellar tendinopathy. Sta- arm ratio with alta, with an ICC of 0.18 (P ¼ .07). tistically significant results (P < .05) were compared with the Insall-Salvati ratio to check for correlations among variables via ICCs. SPSS (v 25; IBM) was used to perform DISCUSSION these statistical analyses. The present study is the first to analyze the sagittal plane biomechanics of the extensor mechanism to identify mor- RESULTS phologic intrinsic risk factors of patellar tendinopathy. Measurements were obtained from planar lateral radio- Measurement Reliability graphs of patients with patellar tendinopathy and were compared with controls. A statistically significant differ- The ICCs for each variable as it was tested between obser- ence in the lever arm and moment arm was found for vers are presented in Table 1, and they revealed strong patients with patellar tendinopathy relative to control

 The Orthopaedic Journal of Sports Medicine Biomechanics in Patellar Tendinopathy 5

TABLE 2 Differences Between Tendinopathy and Control Groups

Mean (SD) 95% CI

Tendinopathy Control Difference Lower Upper P Valuea

Age, y 23.23 (4.71) 23.17 (5.85) –0.04 –2.10 2.02 .97 Maleb 85 55 30 — — <.01 Lever arm 1.71 (1.64) 1.01 (0.43) –0.70 –1.16 –0.23 .01 Moment arm 1.00 (0.34) 0.80 (0.17) –0.20 –0.31 –0.10 <.01 Patellar tendon angle 47.76 (7.14) 47.07 (8.24) –1.08 –4.07 1.90 .59 Pivot point angle 107.94 (10.23) 110.65 (10.71) 2.20 –1.86 6.25 .80 Knee angle 56.13 (19.98) 59.32 (19.65) 2.57 –5.10 10.24 .96 Altab 63 51 12 — — .52

aStatistically significant variables are presented in bold (P < .05). bNominal variables presented as percentages.

Figure 4. Box plot for lever arm ratio between those with and Figure 5. Box plot for moment arm ratio for those with and those without patellar tendinopathy. A statistically significant those without patellar tendinopathy. A statistically significant difference was identified between the lever arm of patients with difference was identified between the moment arm of patients tendinopathy and without. Spread of the data as demonstrated with tendinopathy and without. Spread of data demonstrated through box plot, with the upper and lower limits of the values through box plot, with the upper and lower limits of the values from the horizontal lines and outliers (indicated by patient num- from the horizontal lines and outliers (indicated by patient ber) demonstrated outside. Upper and lower ends of the box number) demonstrated outside. Upper and lower ends of the signify the 75th and 25th percentile, respectively, and median box signify the 75th and 25th percentile, respectively, and between. All data were included in the final analysis. median between. All data were included in the final analysis. patients. Patients with patellar tendinopathy had a patel- angle between the control and tendinopathy groups. The scat- lar lever arm that was smaller relative to the quadriceps ter plot (Figure 6) did not show a strong linear relationship lever arm, while the patellar tendon moment arm length between lever arm ratio and knee flexion angle. Further was smaller relative to the quadriceps moment arm. Draw- research to explore this relationship between the lever arm ing from the work of Huberti et al9 and van Eijden et al,19-21 and the angle of knee flexion is warranted. We were unable to we infer that those with patellar tendinopathy will experi- report normal and abnormal values for different ranges of ence greater force through their patellar tendon as com- knee flexion angle based on the patients reviewed in our pared with those without the condition, owing to the study. Van Eijden et al19-21 explored the relationship of patel- relationship of the patella relative to the femur. lar tendon length on patellar tendon force. The authors Huberti et al9 and van Eijden et al19-21 also reported that reported that patellar tendon length indirectly influences the point of articulation on the patella and femur, what we patellar tendon force by changing the pivot point. However, termed the pivot point in the current study (see Figure 1A), in the current study, we did not find a statistically significant changes with knee flexion angle. However, there was no sta- difference in patella alta between patients with and those tistically significant difference in mean ± SD knee flexion without tendinopathy (post hoc power analysis confirmed

 6 Dan et al The Orthopaedic Journal of Sports Medicine

Figure 6. Scatter plot for lever arm ratio vs knee flexion angle. Visually, no clear relationship is determinable between lever arm ratio (y axis) and knee flexion angle (x axis) for patients included in the present study.

85% power to detect a mean difference of 12 for 100 patients). accept the radiograph, which meant that we had a wide We also did not find a correlation between lever or moment range of knee flexion angles. To account for this, we per- arm with patella alta. This may explain, in part, why previous formed subanalysis by knee flexion angle, and the statisti- studies have failed to show a direct relationship between cal significance of variables did not change, nor did the patella alta and patellar tendinopathy.6,15 relative magnitude of difference. The quality of the lateral In agreement with the work of Schmid et al,16 we did not knee radiograph may also affect the measurements, as the find a difference in patellar tendon angle between controls visual relationship between the trochlea and patella and patients with patellar tendinopathy. Our new mea- changes based on projection changes with rotational differ- surement of patellar tendon pivot point angle aimed to look ences. We did not find this to be an issue in our study. for a combined effect of patellar tendon angle and patellar Additional further research to define normal values for tendon lever arm, but it did not demonstrate a difference. A lever and moment arm ratios for a range of knee flexion post hoc power analysis showed that for a standard devia- angles could be considered, as we did not find a strong tion of 5 and with 100 patients, we could have detected 2 of linear relationship between lever arm ratio and knee flex- mean difference in patellar tendon angle. Therefore, the ion angle (see Figure 6); therefore, we are unable to report relative moment and lever arms were the only statistically normal and abnormal values for different ranges of knee significant biomechanical differences found. flexion angle based on single patient images. These intrinsic differences in anatomy may explain the Altering the lever arm and moment arm ratios could be a subset of patients who do not improve clinically despite treatment option for patellar tendinopathy. A distalizing exhausting current treatment options. The potential clini- tibial tubercle osteotomy alters the point of articulation of cal implication of considering lever and moment arm differ- the patella on the femur by moving it proximally on the ences is 2-fold—specifically, in terms of prevention and patella earlier in the knee flexion range. This change in the treatment. Radiographic screening of athletes in high-risk articulation point, pivot point, and fulcrum of the patella sports (eg, volleyball and basketball) may allow identifica- can manipulate the patellar tendon:quadriceps tendon tion of those who are biomechanically predisposed to devel- force ratio and result in a decrease in the force through the oping the condition, based on lever arm differences. patellar tendon and a relative increase of the force through Training loads and appropriate prehabilitation can be the quadriceps tendon earlier in the knee range of motion— tailored to the individual athlete to try to prevent the the range that is associated with running, jumping, and condition. landing. Further biomechanical work is needed to quantify A limitation of this study, being retrospective, is that we this effect and to ensure that patellofemoral articular forces were not able to (1) control the degrees of flexion in which are not substantially increased before implementation of the knee radiograph was taken and (2) choose whether to any clinical intervention.

 The Orthopaedic Journal of Sports Medicine Biomechanics in Patellar Tendinopathy 7

Intra- and interobserver reliability testing in the current 2. Almekinders LC, Weinhold PS, Maffulli N. Compression etiology in study showed excellent retestability across all measurements. tendinopathy. Clin Sports Med. 2003;22(4):703-710. The use of computer software to accurately and consistently 3. Basso O, Amis AA, Race A, Johnson DP. Patellar tendon fiber strains: perform the measurements may have aided measurement their differential responses to quadriceps tension. Clin Orthop Relat Res. 2002;400:246-253. reproducibility. We identified and marked the anatomic land- 4. Blazina ME. Jumper’s knee. Orthop Clin North Am. 1973;4(3): marks on the lateral radiographs, as described in the figures, 665-678. from which the software performed the subsequent calcula- 5. Dan M, Parr W, Broe D, Cross M, Walsh WR. Biomechanics of the tions for angle and ratio measurements. This removed the user knee extensor mechanism and its relationship to patella tendinopathy: error compounded by repeated measurements. a review [published online August 3, 2018]. J Orthop Res. doi:10. Patient age between groups was similar (see Table 2), but 1002/jor.24120 there was a statistically significant between-group difference in 6. Ferretti A. Epidemiology of jumper’s knee. Sports Med. 1986;3(4): 289-295. patient sex. We chose not to match for sex but instead included 7. Ferretti A, Puddu G, Mariani PP, Neri M. The natural history of jum- appropriate patients as presented by the computer algorithm, per’s knee. Int Orthop. 1985;8(4):239-242. as described in the methods of our screening process, to mini- 8. Hansen P, Haraldsson BT, Aagaard P, et al. Lower strength of the mize selection bias. The sex difference was analyzed and human posterior patellar tendon seems unrelated to mature collagen revealed significant differences that were similar in magni- cross-linking and fibril morphology. J Appl Physiol. 1985;108(1): tude, which suggests that this analysis was not sex specific. 47-52. This study is limited, given the retrospective and nonran- 9. Huberti HH, Hayes WC, Stone JL, Shybut GT. Force ratios in the domized nature, which means that we inevitably introduced quadriceps tendon and ligamentum patellae. JOrthopRes.1984; 2(1):49-54. issues pertaining to selection bias. We tried to minimize this 10. Insall J, Salvati E. Patella position in the normal knee joint. Radiology. by separating patient identification and grouping from the 1971;101(1):101-104. measurement phase of the study, which was done on 11. Johnson DP, Wakeley CJ, Watt I. Magnetic resonance imaging of deidentified data. Furthermore, repeatability measure- patellar tendonitis. J Bone Joint Surg Br. 1996;78(3):452-457. ments were performed independently of each investigator. 12. Lavagnino M, Arnoczky SP, Elvin N, Dodds J. Patellar tendon strain is The present study is based on MRI reports and images, increased at the site of the jumper’s knee lesion during knee flexion with no clinical diagnosis. Johnson et al11 showed that and tendon loading: results and cadaveric testing of a computational model. Am J Sports Med. 2008;36(11):2110-2118. imaging findings correlate poorly with symptoms between 13. Lavernia C, D’Apuzzo M, Rossi MD, Lee D. Accuracy of knee range of asymptomatic and symptomatic individuals. However, the motion assessment after total knee arthroplasty. J Arthroplasty. 2008; current study examined only patients who presented for 23(6):85-91. imaging for a clinical indication of “knee pain”; we excluded 14. Lian OB, Engebresten Bahr R. Prevalence of jumper’s knee among patients who demonstrated other MRI pathology, which elite athletes from different sports: a cross-sectional study. Am J could have confounded the clinical indication for MRI. Sports Med. 2005;33(4):561-567. Therefore, in the absence of other imaging findings, we 15. Roels J, Martens M, Mulier JC, Burssens A. Patellar tendinitis (jum- deduce that the reason for the referral of the included indi- per’s knee). Am J Sports Med. 1978;6(6):362-368. 16. Schmid MR, Hodler J, Cathrein P, Duewell S, Jacob HA, Romero J. Is viduals with only patellar tendinopathy on MRI was impingement the cause of jumper’s knee? Dynamic and static mag- because of a clinical indication for this pathology; however, netic resonance imaging of patellar tendinitis in an open-configuration it is not certain that these patients were truly symptomatic. system. Am J Sports Med. 2002;30(3):388-395. 17. Tyler TF, Hershman EB, Nicholas SJ, Berg JH, McHugh MP. Evidence of abnormal anteroposterior patellar tilt in patients with patellar ten- CONCLUSION dinitis with use of a new radiographic measurement. Am J Sports Med. 2002;30(3):396-401. This study investigated differences in extensor mechanism 18. van der Worp H, van Ark M, Roerink S, Pepping GJ, van den Akker- biomechanics between patients with patellar tendinopathy Scheek I, Zwerver J. Risk factors for patellar tendinopathy: a sys- and control participants, which had not previously been tematic review of the literature. Br J Sports Med. 2011;45(5): reported with lateral radiographs. We identified relative dif- 446-452. 19. van Eijden TM, de Boer W, Weijs WA. The orientation of the distal part ferences in the patellar tendon to quadriceps tendon lever and of the quadriceps femoris muscle as a function of the knee flexion- moment arms. Based on measurements from lateral radio- extension angle. J Biomech. 1985;18(10):803-809. graphs, the patellar tendon had smaller lever and moment 20. van Eijden TM, Kouwenhoven E, Verburg J, Weijs WA. A mathemat- arms among patients with patellar tendinopathy versus con- ical model of the patellofemoral joint. JBiomech. 1986;19(3): trols. We hypothesize that these lever and moment arm dif- 219-229. ferences may result in a greater force through the patellar 21. van Eijden TM, Kouwenhoven E, Verburg J, Weijs WA. Mechanics of tendon of patients with patellar tendinopathy. Further bio- the patellar articulation. Effects of patellar ligament length studied mechanical and clinical studies are needed to test the effect of with a mathematical model. Acta Orthop Scand. 1987;58(5): 560-566. increasing the patellar tendon lever or moment arm. 22. Visnes H, Bahr R. Training volume and body composition as risk factors for developing jumper’s knee among young elite volleyball REFERENCES players. Scand J Med Sci Sports. 2013;23(5):607-613. 23. Witvrouw E, Bellemans J, Lysens R, Danneels L, Cambier D. Intrinsic 1. Almekinders LC, Vellema JH, Weinhold PS. Strain patterns in the risk factors for the development of patellar tendinitis in an athletic patellar tendon and the implications for patellar tendinopathy. Knee population: a two-year prospective study. Am J Sports Med. 2001; Surg Sports Traumatol Arthrosc. 2002;10(1):2-5. 29(2):190-195.

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Knee Surgery, Sports Traumatology, Arthroscopy (2020) 28:975–983 https://doi.org/10.1007/s00167-019-05611-2

KNEE

Sagittal patellar flexion angle: a novel clinically validated patellar height measurement reflecting patellofemoral kinematics useful throughout knee flexion

Michael J. Dan1 · James McMahon2 · William C. H. Parr1 · Nancy Briggs1 · Samuel MacDessi3 · Bruce Caldwell4 · William R. Walsh1

Received: 10 January 2019 / Accepted: 1 July 2019 / Published online: 9 July 2019 © European Society of Sports Traumatology, Knee Surgery, Arthroscopy (ESSKA) 2019

Abstract Purpose Patellar height measurements on lateral radiographs are dependent on knee flexion which makes standardisation of measurements difficult. This study described a plain radiographic measurement of patellar sagittal height which reflects patellofemoral joint kinematics and can be used at all degrees of flexion. Methods The study had two parts. Part one involved 44 normal subjects to define equations for expected patellar position based on the knee flexion angles for three new patellar height measurements. A mixed model regression with random effect for individual was used to define linear and polynomial equations for expected patellar position relating to three novel measurements of patella height: (1) patellar progression angle (trochlea), (2) patellar progression angle (condyle) and (3) sagittal patellar flexion. Part two was retrospective and involved applying these measurements to a surgical cohort to identify differences between expected and measured patellar position pre- and post-operatively. Results All three measurements provided insight into patellofemoral kinematics. Sagittal patellar flexion was the most useful with the least residual error, was the most reliable, and demonstrated the greatest detection clinically. Conclusions Clinically applied radiographic measurements have been described for patellar height which reflect the sagittal motion of the patella and can be used regardless of the degree of flexion in which the radiograph was taken. The expected sagittal patellar flexion linear equation should be used to calculate expected patellar height. Level of evidence IV.

Keywords Patella · Patellar height · Patellar instability · Patellar dislocation · Patella alta

Introduction relationships which are also not reflective of patellofemo- ral kinematics or kinetics [9, 10, 14, 17]. The exception to Patellar height was first described by Blumensaat [8]. ‘Direct this is the patellotrochlear index [4, 6], which relates the measurements’ describe patellar height measurements rela- percentage of the patella engaged with the trochlea, though tive to its position to the femur [22]. These measurements this index has other limitations (most notably that it requires use complicated anatomical landmarks to form angles and lateral radiographs taken in the non-standardised position of knee extension). Conversely, most patellar height measure- ments require a lateral radiograph to be taken at a particular * Michael J. Dan degree of knee flexion, most commonly 30 degree of flexion, [email protected] to which ‘normal’ and ‘abnormal values’ have been refer- 1 Surgical and Orthopaedic Research Laboratory, Prince enced. If taken outside the suggested degree of knee flexion, of Wales Hospital, Prince of Wales Clinical School, the value measured for patellar height will change. University of NSW, Barker St, Randwick 2052, NSW, Clinicians are primarily concerned with patellar height Australia with respect to instability and patellofemoral joint reaction 2 Royal Prince Alfred Hospital, Sydney, NSW, Australia forces for pain [12]. Patellofemoral joint reaction force 3 Sydney Knee Specialists, Kogarah, NSW, Australia (PFJRF) is determined by (1) the contact area between 4 Lingard Hospital, Merewether, Australia the patella and the femur and (2) the force vectors of the

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976 Knee Surgery, Sports Traumatology, Arthroscopy (2020) 28:975–983 quadriceps and patellar tendons. PFJRF is influenced by trochlea for a given knee flexion angle compared to the the morphology of the femur and patella, and changes with normal population (Fig. 1). different degrees of knee flexion. PFJRF is only indirectly This study describes and investigates a new patellar influenced by the patellar tendon length and the tuberosity height measurement for the lateral radiograph which (1) position, which are also variable from patient to patient reflects the kinematics of the patellofemoral joint and (2) can [30, 31]. From an instability point of view, the position be used for any lateral radiograph regardless of the degree of the patella relative to the trochlea is important as, once of the knee flexion in which the radiograph was taken. To engaged, the trochlea is the greatest anatomical restraint accomplish this we planned to exploit the known predictable to dislocation [25]. relationship between the knee flexion angle and the sagit- Kinematics refers to the motion of objects; when con- tal patellar movements of (1) flexion and (2) translation [3, sidering patellar kinematics, the patellofemoral joint has 13, 15, 31]. The aim of the study was for any knee radio- 6 degrees of freedom of movement. Considered in the graph, regardless of the degree of knee flexion, to define the sagittal plane, the patella undergoes a variable amount of expected patellar height position. translation and flexion (also described as sagittal tilt or rotation). Sagittal plane translation and rotation occur in a predictable fashion throughout the knee flexion cycle Materials and methods [3, 13, 15, 31]. Based on this, it was hypothesised that a linear relationship between patellar position and knee The study was done in agreement with the ethical standards flexion angle exists. Subsequently, an individual’s patella of the University of NSW ethics committee (ID HC180217) sagittal plane kinematics will change based on the patella’s and in line with the 1964 Helsinki declaration. Patients gave distance from the trochlea, so that those with patellar alta written consent to participate. The study had two parts. Part will have a different patellar position with reference to the one was prospective and involved defining an equation to

Fig. 1 Sagittal patellar kinematics and study hypothesis. a In the sag- for rotation (R), translation (T) and arc of motion with respect to the ittal plane the patellar undergoes a predictable motion with respect patellar’s centre of rotation (Θ) are expressed in capitals and differ- to knee flexion consisting of b translation (T) and rotation (R). If the ence in size to reflect comparative differences in magnitude for the patella sits in a high position with respect to the trochlea (patellar normal patellar height (c) and patellar alta (d). We aimed to calculate alta), it will undergo a greater amount of translation (T), less rotation an equation to express normal radiographic patellar height for any (r), and progress less in relation to the centre of rotation (o) of the given knee flexion angle based on these kinematic principles patella (Θ) compared to normal subjects. Comparative magnitudes 1 3

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Knee Surgery, Sports Traumatology, Arthroscopy (2020) 28:975–983 977 describe the expected sagittal patellar position based on the Figures 2 and 3 present the patellar progression angle. knee flexion angle at the time of the radiograph for healthy They describe the patella’s angle of progression through normal subjects. 3 new patellar height measurements are flexion with reference to the centre point of rotation in the described utilising this approach (outlined in the following sagittal plane. The centre point of rotation is based either sections). The first part involved recruiting healthy normal from the trochlea (Fig. 2) or the femoral condyle (Fig. 3). subjects and recording fluoroscopic data through the entire The centre of the circle forms the centre of rotation. The cir- range of knee flexion. Subsequently, the new measurements cles are made with reference to the trochlea outline (Fig. 2) for patellar height were performed and formulated an equa- or the femoral condyle (Fig. 3). Sagittal patellar flexion tion to calculate the new patellar height measurement (Y) angle describes the angle formed between the patellar articu- based on a given knee flexion angle (X). lar surface and the posterior condyle of the femur (Fig. 4). Part two was retrospective and applied these novel equa- The knee flexion angle is based off the posterior cortex of tions for expected patellar height in patients with known the tibia and femur [21]. instability who had been operatively treated. The expected patellar position equation was applied to the pre-operative Part one radiograph to determine its sensitivity in detecting patents who underwent a distalising tibial tubercle osteotomy for Healthy volunteers from amateur sporting clubs were instability. The equation was applied to the post-operative recruited and consented to form the normal population. Sub- radiograph to determine sensitivity of those who improved jects were included if they were greater than 16 years of age clinically. (skeletally mature) and less than 35, they did not have any pre-existing knee pathology nor had any previous surgery to the knee. They needed a Kujala score of 100 [18]. Subjects Description of the new patellar height were also excluded if for any other reason, they could not measurements undergo radiographic studies. Fifty patients were recruited for part one. Four were Figures 2, 3 and 4 describe the three new measurements for excluded prior to undergoing radiographic study for the patellar height. These figures describe patella position with following reasons; pregnancy (1), abnormal Kujala score reference to the femur based on the patella sagittal kinemat- (2) and knee pathology/pain (1). 46 patients had fluor- ics involving (1) flexion/tilt/rotation and (2) translation [3, oscopy screening performed; 2 patients were excluded 13, 15, 31]. following completion of imaging due to radiographic

Fig. 2 Patellar progression angle (trochlea). The first step is to define the COR to the midpoint of the patellar articular surface, the angle the centre of rotation (COR). This is done by fitting a circle to the formed between this line and the PL is the patellar progression angle trochlea. To do this, 3 lines of equal length are drawn from different (trochlea) (α). If α is formed proximal to the PL it is assigned a nega- points along the trochlea and the point at which they converge marks tive value. The knee flexion angle (β) is formed by the angle formed the centre of the circle. A line is drawn perpendicular to the poste- between lines drawn along the posterior cortex of the femur and the rior femoral cortex to intersect the COR (PL). A line is drawn from tibia 1 3

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978 Knee Surgery, Sports Traumatology, Arthroscopy (2020) 28:975–983

Fig. 3 Patellar progression angle (condyle). The first step is to define the COR to the mid-point of the patellar articular surface, the angle the centre of rotation (COR). This is done by fitting a circle to the formed between this line and the PL is the patellar progression angle femoral condyle including the trochlea. To do this, 3 lines of equal (condyle) (θ). If θ is formed proximal to the PL, it is assigned a nega- length are drawn from different points along the femoral condyle, one tive value. The knee flexion angle (β) is formed by the angle formed point being the trochlea, and the point at which they converge marks between lines drawn along the posterior cortex of the femur and the the centre of the circle. A line is drawn perpendicular to the poste- tibia rior femoral cortex to intersect the COR (PL). A line is drawn from

Fluoroscopy of the knee as it actively moved from exten- sion to full flexion was performed. Rotation and alignment were matched to ensure overlapping of the medial and lat- eral femoral condyles in accordance with standard lateral radiographs. Static images were produced from the dynamic fluoroscopy throughout the range of motion. Fifteen images for each subject were then selected, which reflected the total range of motion for the knee. Selection was done visually without measurements, aiming to have evenly spaced images across this range, image 1 being maximum extension and image 15 being maximum flexion. The new measurements for patellar height were performed, as well as accurate meas- urements for the knee flexion angle for each image. The software written in Wolfram’s Mathematic language (version 10.1) was used to perform the new patellar height measurements. The software allowed the examiners to place markings representing the points identified in Figs. 2, 3 and 4 before the programme would calculate the measurements Fig. 4 Sagittal patellar flexion angle. The sagittal patellar flexion angle (δ) is the angle subtended by the lines of the patellar articular described for each image. The radiographs were indepen- surface and the posterior cortex of the femur. The knee flexion angle dently reviewed and marked to calculate the described meas- (β) is the angle subtended by the lines drawn along the posterior cor- urements by two blinded examiners (orthopaedic registrars). tex of the femur and the tibia Part one statistical analysis abnormalities (i.e. Osgood–Schlatter’s disease). This left A linear mixed model was employed with random intercept us with a total of forty-four normal subjects. The subjects for person to obtain linear and polynomial equations for had a mean age of 22 years, ranging from 17 to 34 years. the relationship between knee flexion and the new patel- There were 18 females (41%) and 26 males (59%). lar height measurements. Optimal break points for a linear 1 3

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Table 1 Intra- and inter-observer reliability measured knee flexion angle for the given radiograph into Measure Intra-observer Inter-observer the described equations for patellar height (Figs. 5, 6 and 7). These measurements were done both before and after a Progression (trochlea) 0.97 0.98 distalising tibial tubercle osteotomy. Of the two surgeons Progression (condyle) 0.97 0.98 Tilt 0.98 0.99

Intra-observer and inter-observer reliability reported as intraclass cor- relation coefficient (ICC) to 2 decimal places relationship were estimated using the optimise function in R for Part 1 of the study. The inter-observer reliability was compared for all radiographs. In addition, 20 radio- graphs were randomly selected to be remeasured by the first observer to assess intra-observer reliability. Reliability was tested using intraclass correlation coefficient with a two-way mixed model. See Table 1. Post hoc power analysis was performed. With a sample size of 44 patients, and a regression equation including one predictor (linear equation) there was greater than 80% power to detect a moderate effect size, and 90% power to detect a moderate to large effect size. This means that the study was able to detect a linear relationship between knee Fig. 5 R2 Patellar progression angle (trochlea) versus knee flexion flexion angle and patella position assuming an of 0.2. angle. Dots represent individual measurements for the—patellar 2 The observed R for our model was 0.88 patella progres- progression angle (trochlea) and the measured knee flexion angle. sion angle (lowest R2) and for sagittal patellar flexion angle Polynomial curve (red) Y = − 30.91 + 1.62 × KF + − 0.0045 × KF2. was 0.93 (highest R2), meaning our models are more than Residual SD 13.36 valid for all flexion range. The linear relationship Y = − 26.66 + 1.22 × KF. Residual SD 6.82, lower limit knee flexion adequately powered to detect a linear relationship between 1.23° to upper limit 97.89°. Y patellar progression angle (trochlea), patellar position and knee flexion angle. KF knee flexion, SD standard deviation Table 1 shows the intra- and inter-observer reliability, sagittal patellar flexion had the highest intra- and inter- observer reliability.

Part two

The second part of the study was retrospective. Patients who had had a tibial tubercle osteotomy, involving some portion of distalisation were identified. This was done by searching the medical records of two surgeons for the billing code for tibial tubercle osteotomy and screening the operation reports. Patients were excluded if they did not have acces- sible radiographs, or an outcome score completed pre-opera- tively or 12 months post-operatively. This left us with a total of 31 patients with pre- and post-operative radiographs and patient-reported outcome scores following a tibial tubercle osteotomy which included distalisation. The mean age was 16 years, with a range 15–49. There were 20 females (68%) Fig. 6 Patellar progression angle (condyle) versus knee flexion and 11 males (32%). Due to surgeon difference, 14 patients angle. Dots represent individual measurements for the patellar pro- had a Kujala (45%) and 17 had a KOOS (55%). gression angle (condyle) and the measured knee flexion angle. This part of the study involved calculating the differ- Polynomial curve (red) Y = − 28.22 + 1.34 × KF− 0.0031 × KF2. ence between the expected normal patellar position com- Residual SD 6.43 valid for all flexion range. The linear relationship Y = − 23.60 + 1.02 × KF. Residual SD 7.05, lower limit knee flexion pared to the actual measured patellar position. The expected − 16° to upper limit 104.85°. Y patellar progression angle (condyle), normal patellar position is calculated by inputting the KF knee flexion, SD standard deviation 1 3

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Table 2 Expected Patellar Position for given knee flexion angle

Knee Patellar pro- Patellar pro- Sagittal patellar flexion gression angle gression angle flexion angle angle (trochlea) (condyle)

10 − 14.5 − 13.4 9.3 20 − 2.3 − 3.2 16.7 30 9.9 7 24.1 40 22.1 17.2 31.5 50 34.3 27.4 38.9 60 46.5 37.6 46.3 70 58.7 47.8 53.7 80 70.9 58 61.1 90 83.1 68.2 68.5

Examples of the expected patellar position for a given knee flexion angle. These values are calculated by inputting the measured knee flexion angle into the linear equations listed in Figs. 5, 6, 7 Fig. 7 Sagittal patellar flexion versus knee flexion angle. Dots represent individual measurements for the sagittal patellar flex- ion angle and the measured knee flexion angle. Polynomial curve standard deviation when compared to the polynomial equa- (red) Y = 5.89 + 0.42 × KF + 0.0065 × KF2 + 0.000037 × KF3. Resid- ual SD 3.57, valid for all flexion range. The linear relationship tions, with sagittal patellar flexion having the lowest residual Y = 1.94 + 0.74 × KF. Residual SD 3.59, lower limit knee flexion 7.05° standard deviation. A list of expected values for the linear to upper limit 113.18°. Y sagittal patellar flexion, KF knee flexion, equations, based on varying knee flexion angles, is given SD standard deviation in Table 2. involved, one collected Kujala [18], the other the Knee Part 2 Injury and Osteoarthritis Outcome Score (KOOS) [23]. The three linear equations were applied to the radiographs Part two statistical analysis of the patients who underwent a tibial tubercle osteotomy involving distalisation both pre-operatively and post-opera- A two-tailed paired Student’s t test was utilised to compare tively. The measured knee flexion angle that the radiograph differences in patient-reported outcome scores and radio- was taken in was used to calculate the expected patellar posi- graphic measurements pre- and post-operatively in Part two. tion for each patient. Three measurements of the patellar Statistical analysis was performed using R-3.5.1 statistical height were also performed. package. The difference between this measured patellar height Post hoc power analysis revealed a power of greater than position and expected patellar position (based on knee 80% power to detect a linear relationship between knee flex- flexion angle of the radiograph) for the measurements was ion angle and sagittal patellar position, and to show differ- compared post-operatively to pre-operatively. There was a ences between normal and patellar alta subjects (part 2) for mean difference of 14.2°, range 6.78–21.62, for progression all measurements. angle (trochlea) (P < 0.001). There was a mean difference of 12.53°, range 5.19–19.87, for patellar progression (condyle) (P = 0.002). There was a mean difference of 23.55, range Results 19.50–27.60, for sagittal patellar flexion (P < 0.001). Patellar alta was present in 90.3% (28) of patients as per Part one—normal population the Insall-Salvati ratio (i.e. patellar tendon length to patella length greater than 1.2). Residual standard deviation (RSD) Figures 5, 6, and 7 demonstrate the distribution of normal was used for each equation defined in Figs. 4, 5 and 6 to values across a range of knee flexion angles, along with the define patellar alta. The sensitivity of the measurement was polynomial and the linear equation for patellar progression determined by those patients who had a measured patellar angle (trochlea), patellar progression angle (condyle) and height greater than one and two standard deviations from the sagittal patellar flexion, respectively. Figures 5, 6 and 7 also expected normal value based on the measured knee flexion explain the residual standard deviation for each measure- angle for the radiograph (Table 3). Sagittal patellar flexion ment and the range of knee flexion angles for which the identified most patients with an abnormal result pre-opera- equations are valid. The linear equations had similar residual tively and the least with an abnormal result post-operatively. 1 3

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Table 3 Percentage of patients with patellar alta patients but not in normal controls when comparing patellar Measurement Pre op Post op height with weight bearing and non-weight bearing images. It is noted that weight bearing changes hip position as well. 1 RSD 2 RSD 1 RSD 2 RSD Laugharne et al. [19] positioned the patients in the same way Progression-trochlea RSD = 6.82 77.4 54.8 35.4 16.1 as in our study and compared active to inactive quadriceps Progression-condyle RSD = 7.05 80.7 51.6 22.6 9.7 and reported this difference to be negligible and potentially Sagittal patellar flexion RSD = 3.59 83.9 77.4 0 0 within the margin of error for this measurement. The new radiograph measurements described here are SD refers to residual standard deviation. See Figs. 5, 6 and 7 for based on the patella rotating around a common centre point each measurements residual standard deviation. Alta determined by measured patellar measurement being greater than 1 or 2 SDs from [15], and are based on the known linear relationship between the expected patellar measurement angle for the given angle of knee the sagittal patellar position and knee flexion angle [3, 29]. flexion the radiograph was taken in. RSD residual standard deviation The progression angle was calculated based on two cen- tre points of rotation. The condylar-based point (Fig. 3) was found to be similar to Schottle’s point [24]. This is the There was an improvement in patient-reported outcome radiographic landmark for isometric position of a medial score of 25.2 points, range 19.5–31.0 (P < 0.001). The mean patellofemoral ligament reconstruction, which equates to a difference was near identical at 24.6 (P < 0.001) for Kujala centre of rotation of the patella. The trochlea-based centre and 25.8 (P < 0.001) for KOOS pain. point of rotation changes based on the shape of the trochlea, with a dysplastic trochlea having a flatter radius of curvature [32]. Given that we performed a ‘within-subjects repeated Discussion measures analysis’ in our regression analysis to calculate our equations, individual trochlea shape variability was The most important finding of this study was that the 3 patel- accounted for. While there are also gender-based differ- lar height measurements based on patellofemoral kinemat- ences between the patellar tracking [33], different equations ics can be used regardless of the degree of knee flexion the for gender were not included to reduce complexity of the radiograph was taken in and demonstrated a great clinical measurements. correlation to pre- and post-operative radiographs for tibial Sagittal patellar flexion is not an entirely new concept. tubercle osteotomy with distalisation. Three new measure- Tyler et al. [27] identified differences between normal ments for assessing patellar height on lateral radiographs patients and patellar tendinopathy based on the patellar tilt were described. These measurements reflect the sagittal referenced to the anterior femoral cortex. Aksahin et al. iden- plane patellar kinematics which occurs through knee flexion, tified differences in ‘patella tilt’ in patients with chondroma- that is (1) flexion and (2) translation [3, 13, 15, 31]. Each lacia patella and anterior knee pain post tibial nail. However, method was useful for identifying patients who have symp- patella tilt was defined by the angle between the patellar tomatic instability, indicated by a need for distalisation in the tendon and the superior patellar apex [1, 2]. Sagittal patellar cohort in part 2 of the study. The clinical applicability was position is increasingly investigated in the kinematics and reflected by the large percentage of patients having normal- kinetics of knee arthroplasty [26, 28]. The relationship of ised patellar height measurements post-operatively and the sagittal patellar flexion to knee flexion has been previously corresponding excellent clinical results noted by improved described in radiographic and cadaveric studies [3, 13, 15, patient-reported outcome scores. 31]; however, it has not been correlated with instability. We Based on the available evidence, a seated radiograph with prefer the term sagittal patellar flexion to avoid confusion quadriceps contraction will not differ greatly to a seated radi- with patellar tilt in the axial plane [20]. ograph without quadriceps contraction for our measurements Sagittal patellar flexion was able to identify approxi- of the normal patients but this potential limitation is recog- mately 80% of patients with an abnormal sagittal patellar nised. Patellar instability is largely an active phenomenon flexion and who gained benefit from a distalisation, with (quadriceps contracted). An actively contracted quadriceps subsequent 0% of patients having post-operative patellar alta in a patient with symptomatic patellar alta could have an as determined by the residual standard deviation. While we even higher value outside the normal range, further increas- identified 90.3% of patients pre-operatively with patellar alta ing the sensitivity of this radiographic measurement. It is as per the Insall-Salvati ratio, this by measurement does not important in the future to quantify any potential differences change with a tibial tubercle osteotomy as the length of the between radiographs with quadriceps activation and relaxa- patellar tendon remains intact. tion in the application for the described patellar height meas- The purpose of this study was to redefine sagittal patel- urements in this paper. This is based on the findings from lar position on the lateral radiograph to reflect the correct Becher et al. [5], where differences were found in instability kinematics. It was not to compare our measurements to 1 3

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982 Knee Surgery, Sports Traumatology, Arthroscopy (2020) 28:975–983 traditional measures of patellar height and claim superior- Conclusion ity in identification of patella conditions as these measure- ments indirectly reflect patellar kinematics and kinetics This study has described clinically applied radiographic [30]. It is important, however, to consider how normal measurements for patellar height which reflects the sagit- compared with abnormal results are identified for these tal motion of the patella and can be used regardless of the popular patellar height measurements. There is consider- degree of flexion in which the radiograph was taken. The able overlap between normal subjects and patients with expected sagittal patellar flexion should be used for patel- instability. For example, the Blackburne–Peel ratio has lar height as it demonstrated the least residual error, was been described as 0.92 for instability and 0.81 for nor- the most reliable, had the greatest detection clinically and mal subjects, with standard deviations of 0.21 and 0.14, was the easiest to measure on non-specialised software respectively [7]. This overlap is well known, and extends (cobb angle). Future studies can continue to validate the to other measures such as the Caton–Deschamps, whereby applicability of this measurement to other patellar-related to improve the specificity of the measurement to 100%, clinical entities. a threshold of 1.2 is needed and the Caton–Deschamps measurement sensitivity is reduced to just 24% [11]. We Acknowledgements We would like to acknowledge and thank Debby had a sensitivity of 77%, and specificity of 95%, in detect- Chambers, Dianna Dunn and Jil Wood for coordinating access to patient data and imaging facilities. To Sonya Fisher who gave up time ing patients with instability and a when using 2 RSDs as to perform radiographs for part 1 of the study. the normal range for expected values. Intra- and inter-observer reliability testing showed Funding There was no funding for this project. excellent re-testability across all measurements. The use of computer software to accurately and repeatedly per- Compliance with ethical standards form the measurements may have aided measurement reproducibility. The investigators identified and marked Conflict of interest The author(s) declare that they have no competing the anatomical landmarks on the lateral radiographs and interests. the software performed the subsequent calculations. This Ethical approval The study was done in agreement with the ethical removed the complexity of defining the centre of the circle standards of the University of NSW ethics committee (ID HC180217) and user errors compounded by repeated measurements. and in line with the 1964 Helsinki declaration. The literature for defining new patellar measurements is comparable with the 44 normal patients in this study. However, this study is limited by the fact that there are known differences in anatomy and patellar position across References ethnicities [16]. Another limitation is that given there were no symptomatic patients a reference range to define patel- 1. Aksahin E, Aktekin CN, Kocadal O, Duran S, Gunay C et al lar baja/infera could not be given. The popular measures (2017) Sagittal plane tilting deformity of the patellofemoral of patellar height are easier to measure than our described joint: a new concept in patients with chondromalacia patella. Knee Surg Sports Traumatol Arthrosc 25(10):3038–3045 measurements for the trochlea and condyle patellofemoral 2. Aksahin E, Yilmaz S, Karasoy I, Duran S, Yuksel HY et al progression angle. Noting this, we, as the authors, would (2016) Sagittal patellar tilt and concomitant quadriceps hypo- be happy to provide the Mathematica programme to others trophy after tibial nailing. Knee Surg Sports Traumatol Arthrosc wanting to investigate patellar progression angle (trochlea 24(9):2878–2883 3. Amis AA, Senavongse W, Bull AM (2006) Patellofemoral kine- or condyle) in other areas of knee pathology or related matics during knee flexion-extension: an in vitro study. J Orthop to other ethnicity groups to improve applicability. It is Res 24(12):2201–2211 proposed that sagittal patellar flexion angle is a superior 4. Barnett AJ, Prentice M, Mandalia V, Wakeley CJ, Eldridge JD measure and can be calculated without the use of techni- (2009) Patellar height measurement in trochlear dysplasia. Knee Surg Sports Traumatol Arthrosc 17(12):1412 cal software. 5. Becher C, Fleischer B, Rase M, Schumacher T, Ettinger M et al A further limitation was that the clinical application was (2017) Effects of upright weight bearing and the knee flexion done retrospectively, and all patients showed improvement angle on patellofemoral indices using magnetic resonance imag- clinically. The retrospective nature introduces selection ing in patients with patellofemoral instability. Knee Surg Sports Traumatol Arthrosc 25(8):2405–2413 bias. It is, however, a good initial start point from which 6. Biedert RM, Albrecht S (2006) The patellotrochlear index: a further application can be done prospectively to validate the new index for assessing patellar height. Knee Surg Sports Trau- measurement for other normal and pathological populations, matol Arthrosc 14(8):707–712 along with correlation between the radiographic measure- 7. Blackburne JS, Peel TE (1977) A new method of measuring patellar height. J Bone Jt Surg Br 59(2):241–242 ment and patients who improve, fail to improve or are made worse with surgery. 1 3

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8. Blumensaat C (1938) Die lageabweichungen und verrenkungen 23. Roos EM, Roos HP, Lohmander LS, Ekdahl C, Beynnon BD der kniescheibe. In: Payr E, Kirschner M (eds) Ergebn Chir (1998) Knee injury and osteoarthritis outcome score (KOOS)– Orthop. Springer, Berlin, Heidelberg, pp 149–223 development of a self-administered outcome measure. J Orthop 9. Burgess RC (1989) A new method of determining patellar posi- Sports Phys Ther 28(2):88–96 tion. J Sports Med Phys Fitness 29(4):389 24. Schottle PB, Schmeling A, Rosenstiel N, Weiler A (2007) Radi- 10. Chareancholvanich K, Narkbunnam R (2012) Novel method of ographic landmarks for femoral tunnel placement in medial measuring patellar height ratio using a distal femoral reference patellofemoral ligament reconstruction. Am J Sports Med point. Int Orthop 36(4):749–753 35(5):801–804 11. Dejour H, Walch G, Nove-Josserand L, Guier C (1994) Factors 25. Senavongse W, Amis AA (2005) The effects of articular, retinacu- of patellar instability: an anatomic radiographic study. Knee Surg lar, or muscular deficiencies on patellofemoral joint stability: a Sports Traumatol Arthrosc 2(1):19–26 biomechanical study in vitro. J Bone Jt Surg Br 87(4):577–582 12. Feller JA, Amis AA, Andrish JT, Arendt EA, Erasmus PJ et al 26. Stagni R, Fantozzi S, Catani F, Leardini A (2010) Can patellar (2007) Surgical biomechanics of the patellofemoral joint. Arthros- tendon angle reveal sagittal kinematics in total knee arthroplasty? copy 23(5):542–553 Knee Surg Sports Traumatol Arthrosc 18(7):949–954 13. Hamai S, Dunbar NJ, Moro-oka TA, Miura H, Iwamoto Y et al 27. Tyler TF, Hershman EB, Nicholas SJ, Berg JH, McHugh MP (2013) Physiological sagittal plane patellar kinematics during (2002) Evidence of abnormal anteroposterior patellar tilt in dynamic deep knee flexion. Int Orthop 37(8):1477–1482 patients with patellar tendinitis with use of a new radiographic 14. Hepp WR (1984) 2 new methods for determination of the height measurement. Am J Sports Med 30(3):396–401 of patella. Z Orthop Ihre Grenzgeb 122(2):159–166 28. van Duren BH, Pandit H, Pechon P, Hart A, Murray DW (2018) 15. Iranpour F, Merican AM, Baena FR, Cobb JP, Amis AA (2010) The role of the patellar tendon angle and patellar flexion angle in Patellofemoral joint kinematics: the circular path of the patella the interpretation of sagittal plane kinematics of the knee after around the trochlear axis. J Orthop Res 28(5):589–594 knee arthroplasty: a modelling analysis. Knee 25(2):240–248 16. Karadimas JE, Piscopakis N, Syrmalis L (1982) Patella alta and 29. van Eijden TM, de Boer W, Weijs WA (1985) The orientation of chondromalacia. Int Orthop 5(4):247–249 the distal part of the quadriceps femoris muscle as a function of 17. Koshino T, Sugimoto K (1989) New measurement of patellar the knee flexion-extension angle. J Biomech 18(10):803–809 height in the knees of children using the epiphyseal line midpoint. 30. van Eijden TM, Kouwenhoven E, Verburg J, Weijs WA (1986) J Pediatr Orthop 9(2):216–218 A mathematical model of the patellofemoral joint. J Biomech 18. Kujala UM, Jaakkola LH, Koskinen SK, Taimela S, Hurme M 19(3):219–229 et al (1993) Scoring of patellofemoral disorders. Arthroscopy 31. van Eijden TM, Kouwenhoven E, Weijs WA (1987) Mechanics of 9(2):159–163 the patellar articulation Effects of patellar ligament length studied 19. Laugharne E, Bali N, Purushothamdas S, Almallah F, Kundra R with a mathematical model. Acta Orthop Scand 58(5):560–566 (2016) Variability of measurement of patellofemoral indices with 32. Varadarajan KM, Freiberg AA, Gill TJ, Rubash HE, Li G (2010) knee flexion and quadriceps contraction: an MRI-based anatomi- Relationship between three-dimensional geometry of the trochlear cal study. Knee Surg Relat Res 28(4):297–301 groove and in vivo patellar tracking during weight-bearing knee 20. Laurin CA, Levesque HP, Dussault R, Labelle H, Peides JP (1978) flexion. J Biomech Eng 132(6):061008 The abnormal lateral patellofemoral angle: a diagnostic roentge- 33. Varadarajan KM, Gill TJ, Freiberg AA, Rubash HE, Li G (2010) nographic sign of recurrent patellar subluxation. J Bone Jt Surg Patellar tendon orientation and patellar tracking in male and Am 60(1):55–60 female knees. J Orthop Res 28(3):322–328 21. Lavernia C, D’Apuzzo M, Rossi MD, Lee D (2008) Accuracy of knee range of motion assessment after total knee arthroplasty. J Publisher’s Note Springer Nature remains neutral with regard to Arthroplasty 23(6 Suppl 1):85–91 jurisdictional claims in published maps and institutional affiliations. 22. Phillips CL, Silver DA, Schranz PJ, Mandalia V (2010) The meas- urement of patellar height. J Bone Jt Surg Br 92(8):1045–1053

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 Received: 29 October 2019 | Accepted: 23 April 2020 DOI: 10.1002/jor.24714

RESEARCH ARTICLE

Moment arm function dictates patella sagittal height anatomy: Rabbit epiphysiodesis model alters limb length ratios and subsequent patellofemoral anatomical development

Michael J. Dan | William C. H. Parr | James D. Crowley | Rema A. Oliver | Kimberley Kai Lun | Vedran Lovric | Mervyn Cross | David Broe | William R. Walsh

Surgical and Orthopaedic Research Laboratories (SORL), Prince of Wales Clinical Abstract School, UNSW Sydney, Randwick, New South Wales, Australia Patellofemoral anatomical dysplasia is associated with patellofemoral instability and pain. The closure of the knee physis occurs at the same age as the peak incidence of Correspondence Michael J. Dan, Surgical and Orthopaedic patellofemoral dislocation. This study determined the effect on the patellofemoral Research Laboratory, Prince of Wales Hospital, anatomical development in a rabbit epiphysiodesis model. Twenty‐four skeletally Barker St, Randwick, NSW 2052, Australia. Email: [email protected] immature New Zealand White rabbits were divided into three groups (a) distal femur epiphysiodesis (FE) (b) proximal tibia epiphysiodesis (TE) (c) control; no epi- physiodesis (C) performed at 6 weeks of age. The primary endpoint was shape analysis using three‐dimensional reconstructions of micro‐computed tomographys (CTs) performed at 30 weeks of age. The limb length ratios (femur:tibia) were sig- nificantly different for both FE (mean 0.72, SD 0.0381, P < .001) and TE (mean 0.91, SD 0.0383, P < .001) treatment groups compared to control (mean 0.81, SD 0.0073). Patella height, as measured from the most distal point of the patella to the tibial joint surface (modified Caton‐Deschamps measurement), was lower (baja) in the FE and higher (alta) for the TE, compared with the control group. Our findings suggest femoral and tibial shortening can influence the development of the patellofemoral joint, which may be dictated by moment arm function and is potentially responsible for the etiology of patella alta. Future studies are warranted to explore this asso- ciation further with the view for the development of treatment options for patella alta in human patients.

KEYWORDS patella tendinopathy, patellofemoral

1 | INTRODUCTION surgical procedures have been proposed to address these predis- posing factors in an “a la carte” fashion.1 It is unknown why different Anatomical abnormalities contribute to patellofemoral pain and dis- individuals develop these anatomical abnormalities; is it the chicken location, including trochlear dysplasia, excessive distance between or the egg, or as phrased by Tanaka “which came first, the patella or tibial tubercle and trochlear groove, and patella alta. Corrective the trochlea?”.2 The bi‐convex shape of the patella develops in utero

------© 2020 Orthopaedic Research Society. Published by Wiley Periodicals LLC

J Orthop Res. 2020;1–11. wileyonlinelibrary.com/journal/jor | 1

 2 | DAN ET AL. without compression against the femoral trochlea.3 The femoral isoflurane induction and maintained between 2% and 3%, titrated to trochlea also develops it's characteristic bi‐concave shape in utero by effect. Continuous multiparameter cardiopulmonary monitoring (Datalys 18 weeks,4,5 suggesting this dysplastic predisposition from birth. V7; Lutech, Ronkonkoma, NY) was used throughout anesthesia. The Rabbit research models have been developed to alter the com- rabbits received external heat support in the form of a heat pad. Fol- pression of the patella against the trochlea based on previous research lowing completion of surgery, the rabbits were wrapped in a towel for on the development and treatment of hip dysplasia in humans.6 Rabbit added warmth and received masked oxygen supplementation until models investigating changing patella position through dislocation,7 righting before being returned to their housing pen. Prophylactic anti- reduction or persistent dislocation,8 subluxation due to medial re- biotics (Enrofloxacin 5 mg/kg IM) was provided prior to surgery and tinaculum incision9 or patella alta due to patella tendon lengthening,10 continued for 5 days postoperatively. Carprofen (2 mg/kg s/c) was ad- have all concluded that the less time the patella spends in articulation ministered for postoperative analgesia and inflammation. Buprenorphine with the trochlea, the flatter it develops. This finding suggests a de- (0.02‐0.05 mg/kg IM) was administered for rescue analgesia as indicated. velopmental contribution to pathological patellofemoral anatomy. In The rabbits were monitored daily for the first week postoperative, paying contrast, human studies have suggested that while the magnitude of particular attention to appetite, demeanor, the surgical site and re- the trochlea dimensions change with growth, normal trochlea shape11 quirement for additional analgesia. The rabbits were weighed weekly or dysplasia12 is likely genetically predetermined. prior to euthanasia at 6 weeks postoperative (30 weeks old) via in- This is despite the lack of longitudinal studies in humans in- tracardiac pentobarbitone injection under general anesthesia. vestigating patellofemoral anatomical morphology changes with time/growth. Peak incidence of patellofemoral dislocations occur between the 2.3 | Surgery ages of 15 to 19 years,13,14 which corresponds with closure of the distal femoral and proximal tibial physis.15 Therefore, the objective of All surgical procedures were completed by a senior orthopaedic re- this study was to explore the role of the physis on patellofemoral gistrar (MD) and veterinary surgeon (JC). For all treatment groups, development. We aimed to determine if isolated epiphysiodesis, to both hindlimbs were clipped from the proximal femoral region to the either the distal femoral or proximal tibial physis, the tibia to tarsus and aseptically prepared for surgery (povidine‐iodine solution). femur limb length ratio and subsequently affected development of the The medial stifle was aseptically draped into the sterile field using patellofemoral joint in a rabbit model of skeletally immature animals. disposable, impermeable drapes. A medial skin incision (~3‐5 cm) was made from the parapatellar region to 1 cm distal to the tibial crest. The same skin incision was performed for all animals, regardless of 2 | MATERIALS AND METHODS the treatment group. The physis of interest was approached via a combination of blunt and sharp dissection and located via placement 2.1 | Animals of a 23 g sterile needle, confirmed via a portable fluoroscopy unit (Shanghai Bojin Electric Instrument & Device Co, Shanghai, China). Following approval by the Institutional Animal Care and Ethics The periosteum overlying the physis was sharply incised prior to Committee (ACEC approval 18/45A, NSW, Australia), 24 6‐week‐old physical and heat ablation using a high‐speed motorized burr (Midas female New Zealand White rabbits (Biological Research Centre, Rex, Medtronic, Memphis, TN), as previously described.1,16 Briefly, Sydney, Australia), with a mean weight of 1.2 kg, were equally divided the burr was directed perpendicular to the physis and burring per- and randomly assigned to one of three groups (a) distal femoral formed under high speed in all directions along entire length of the epiphysiodesis (FE) (b) proximal tibial epiphysiodesis (TE), and (c) physis using a fanning motion. To serve as future radiographic re- control; no epiphysiodesis (C). All rabbits were systemically well with ference points, a 0.6 mm Kirschner wire was cut into 1 to 2 mm a normal body condition and no orthopedic or neurological ab- lengths and inserted parallel to the physis in the adjacent distal femur normalities based on examination by a veterinarian (JC). The rabbits and proximal tibial metaphysis in a mediolateral direction for all were acclimatized for 1 week with a maximum of four rabbits per treatment groups. The Kirschner wire lengths penetrated the near pen, housed at 22°C with a 12‐hour day‐night cycle. The rabbits were (cis) cortex only. Fascial and subcutaneous tissues were closed in a maintained on timothy hay straw and commercial pellets (Gordan's simple continuous pattern (3‐0 Vicryl). The skin was closed with in- Specialty Stockfeeds, NSW, Australia), supplemented with fresh dark tradermal sutures (3‐0 Vicryl). All rabbits recovered uneventfully leafy greens and other vegetables. Water was provided ad libitum. from surgery and were returned to their housing pen with no ex- ercise restrictions placed on them for the duration of the study.

2.2 | Anesthesia and perioperative care 2.4 | Diagnostic imaging The rabbits were premedicated with buprenorphine (0.03 mg/kg) and midazolam (0.5 mg/kg) via intramuscular injection using a 26 g insulin Bilateral orthogonal hindlimb radiographs (anterior‐posterior and needle. The rabbits were preoxygenated for 10 minutes prior to masked mediolateral) were performed at 0, 3, 6 and 24 weeks postoperatively

 DAN ET AL. | 3

FIGURE 1 Isolated tibial (above) and femoral (below) articular surfaces. A, tibial tuberosity, B, lateral proximal tibia, C, medial proximal tibia, D, distal tibia (talocrural), E, femoral trochlea, F, medial femoral condyle, H, lateral femoral condyle and I) femoral head [Color figure can be viewed at wileyonlinelibrary.com] under general anesthesia using the previously described anesthetic 2.6 | Morphological analyses—femoral coordinate protocol. Radiographs were processed by a Faxitron (Faxitron Bioptics, system LLC, Arizona) and digital plates (AGFA CR MD4.0 Cassette, AGFA, Germany) at 24 kV over 45 seconds. An AGFA Digital Developer and Spheres and planes were fitted to the articular surfaces identified dedicated workstation was used to process the digital images above using least‐squares minimization. The coordinate system was (AGFA CR 75.0 Digitizer Musica, AGFA, Germany). The DICOM adapted from the International Society of Biomechanics (ISB) re- data was converted to Bitmap images using DICOM Works (ez- commendations.17 Differing from ISB recommendations,17 0,0,0 for DICOM medical viewer, copyright 2002). Physeal closure and the coordinate system was set at the centroid of the distal tibial Kirschner wire positioning were evaluated on all acquired articular surface. The centre of rotation of the hip joint was calcu- radiographs by two blinded observers. lated as the centre point of a sphere fitted to the articular surface of All rabbits underwent helical multidetector micro‐computed to- the femoral head (Figure 2) and was used to define the orientation mographic (micro‐CT) evaluation (resultant slice thickness of 120 μm) (main axis) of the femoral coordinate system. of both hindlimbs at 24 weeks postoperative following euthanasia In contrast to Wu et al,17 spheres were also fitted to the medial (MILabs, Utrecht, the Netherlands). The knee was maintained at 30° and lateral femoral condyles as described previously.18,19 Fitting of flexion for all acquired images, to maintain patella tendon tension. spheres to the femoral condyles should reduce intra‐ and inter‐user error in defining femoral epicondyles.17 The midpoint of the line between the centres of these two spheres was defined (Figure 3); 2.5 | Three‐dimensional reconstruction—segmentation akin to the midpoint of the femoral epicondyles as described by Wu of micro‐CT images et al.17 The y‐axis was defined as the vector between the midpoint be- Three‐dimensional (3D) isosurface boundary representations (b‐reps) tween the femoral condyle fitted spheres and the centre of rotation of the right and left hindlimbs were reconstructed from micro‐CT for the femoral head articular surface. The x‐axis was defined as the DICOM images using Materialize MIMICS vs 19 (Leuven, Belgium). cross product of the y‐axis vector and the vector between the cen- Models were femora, tibia, and patellae from the right hand side tres of the spheres fitted to the medial and lateral femoral condyles. (RHS) and left hand side (LHS) hindlimbs were separated during the The axes were set so that anterior orientation represented a positive segmentation process. Following 3D reconstruction, tibial, femoral value. The z‐axis was defined by taking the cross product of the y and and patella articular surfaces were isolated to enable subsequent x axes and set so that lateral was positive. Once the coordinate analysis (Figure 1). Note that the articular surfaces were maintained system was defined, each specimen was moved so that the centroid in the same position relative to one another. of the tibial talocrural joint surface was at 0,0,0 and rotated so

 4 | DAN ET AL.

Sagittal patella sphere radius, articular glide length and theta were also calculated for the patella using a similar method (Figure 6). As the trochlea and patella articular surfaces are curved in two planes (longitudinal and transverse), central strips of these facets were isolated and fitted with 2D (Figure 5) and 3D (Figure 6) circles/ spheres to capture the longitudinal curvature (the major axis cur- vature) for analysis. Using the central strip allows identification of the centre point of rotation during knee flexion and extension, whereas the transverse curvature (trochlea groove depth) is asso- ciated with maintaining the patella in the trochlea groove, thereby preventing dislocation during flexion and extension movements. The goodness of fit of this method is depicted in Figures 5 and 6. To assess the extents of the influence of function (the need to articulate with, and slide across the femoral trochlea articular sur- face) on the anatomy of the patella articular surface curvature, the centre points of rotation for the patella and femoral trochlea ar- ticular surfaces were calculated. If the only constraint on the patella

FIGURE 2 Sphere (purple) fitted to the articular surface (yellow) morphology was to fit with and move across the trochlea, it could be of the RHS femoral head. The calculated centre point of the fitted sphere expected that the centre points of spheres fitted to the major axis is shown [Color figure can be viewed at wileyonlinelibrary.com] curvature of both articular surfaces would be coincidental. To further assess patella height positioning between treatment groups, distances between the patella and the previously defined that the femoral coordinate system was aligned with the global distal femoral and proximal tibial articular surfaces were calculated coordinate system (Figure 4). Femur lengths were calculated as the (Figure 7). We related these measurements to clinically used mea- length of the vector from the centre of the sphere fitted to the surements reflecting the Caton‐Deschamps index,20 Insall‐Salvati femoral head articular surface to the mid‐point between the sphere ratio21 was taken as the distance between the centre of the tibial centre points fitted to the medial and lateral femoral condyles. Tibial patella tendon insertion (red) and the centre of the patella articular lengths were calculated as the mid‐point between the two centroids surface (solid black line). The patella‐trochlea engagement mea- of the proximal tibial articular surfaces (medial and lateral) and the surement22 was defined as the distance between the centre of the centroid of the distal (talocrural) articular surface. patella articular surface and the most superior point of the femoral Femoral trochlea articular glide length was defined as the arc trochlea articular surface (dashed line). The patella tendon length length of a sphere fitted to the femoral trochlea articular surface (dot‐dashed black line) was measured from the inferior pole of the (Figure 5). patella to the centre of the patella tendon insertion on the tibia (red).

FIGURE 3 Spheres (purple) fitted to the medial and lateral femoral condyles (yellow) of the right hindlimb. The medial epicondyle is on the right‐hand side of the figure and the lateral epicondyle is on the left‐hand side of the figure [Color figure can be viewed at wileyonlinelibrary.com]

 DAN ET AL. | 5

Significance was set at an α level of P < .05. All data is presented as the mean and the standard deviation of the mean. Reliability was tested with the intraclass correlation coefficient (ICC) via a two‐way mixed model. Analysis was performed using SPSS version 18.0 for Windows (SPSS Inc, Chicago, IL).

3 | RESULTS

Descriptive statistics for post hoc Tukey's HSD multiple comparison tests are presented in Table 1.

3.1 | Radiographs

For all rabbits in groups FE and TE, postpoperative radiographs de- monstrated successful cessation of growth by the lack of change in the distance between the Kirschner wires and the adjacent ablated physis compared with the continued growth away from the un- affected physis respectively. No other radiographic abnormalities such as fractures and subluxations were noted for any animal at all radiographic time points.

3.2 | Limb length ratios

The limb length ratios (femur:tibia) were significantly different for both group FE (mean 0.72, SD 0.04, P < .001) and group TE (mean 0.91, SD 0.04, P < 0.001) compared with group C (mean 0.81, SD 0.01) (Figure 9).

FIGURE 4 Selected articular surfaces for the left hindlimb oriented within the global coordinate system. The black lines 3.3 | Patellar height represent the tibial and femoral lengths. The angle between the black lines in the xy plane was taken as the flexion angle. The angle between the black lines in the zy plane was taken as the varus‐valgus Patella height, as measured from the most distal point of the patella angle. The y‐axis represents the vertical axis. The x‐axis to the tibial joint surface (modified Caton‐Deschamps index), was represents the horizontal axis [Color figure can be viewed at lower (baja) in group FE and higher (alta) for group TE, compared to wileyonlinelibrary.com] the (Figure 9). The limb length ratio was correlated with the tibial joint surface to The medial and lateral aspects of the patella articular surface patella height measurement (modified Caton‐Deschamps index; were partitioned using a modified watershed algorithm (Figure 8A). ICC = 0.63, P = .01). The patella tendon length was correlated to the Planes were fitted to the medial and lateral aspects of the patella modified Insall‐Salvati index (ICC 0.92, P = .01), while the limb length surface and the angle between the normal vectors of these ratio to Insall‐Salvati index was not (ICC 0.25). This is reflected by two planes was calculated (Figure 8B). group FE having a significantly shorter patellar tendon length (P =.01) and shorter Insall‐Salvati index (P = .04), compared with group C. There was no significant difference between groups C and TE for 2.7 | Statistical analysis patellar tendon length (P =.15)andInsall‐Salvati index (P =.75).

Quantitative parameters between treatment groups were analysed by analysis of variance. A post hoc Tukey's HSD multiple comparison 3.4 | Trochlea curve test was used to detect significant differences between the treat- ment effects. For nonnormally distributed data, nonparametric The trochlea sphere radius was smaller in group FE (mean 14.08 mm, Kruskal‐Wallis tests were used to compare the treatment effects. SD 3.83 mm) compared with group C (mean 14.82 mm, SD 1.72 mm),

 6 | DAN ET AL.

FIGURE 5 Two‐dimensional (2D) representation of the calculation of the femoral trochlea articular surface glide length. Arc length (red) was defined by vectors (blue) from the fitted sphere centre point to the extents of the aligned articular surface. Theta was calculated as the angle between the two extent vectors [Color figure can be viewed at wileyonlinelibrary.com]

however, was not statistically significant (P = .74). The trochlea sphere radius for group TE (mean 15.22 mm, SD 2.15 mm) was greater than group C but was not statistically significant (P = .92). Femoral trochlea length for group FE was significantly shorter than group C (P = .01), however, there was no significant difference between group C and group TE (P = .94). Femoral trochlea theta for group FE (74.71°, SD = 21.11) was significantly smaller than group C (89.44°, SD = 8.18, P = .03), however, there was no significant dif- ference between group C and TE (P = .72). For group FE, the difference in the trochlea and patella centre point of rotation (mean, SD was significantly shorter than the TE (P < .001) and control group (P = .002), however, there was no sta- tistical difference between TE and C (P = .91).

3.5 | Patella

Patella length (P = .58), angle between medial and lateral articular surfaces (P = .77), and sagittal radius of curvature (P = .14) did not differ between treatment groups. Trochlea sphere ratio was correlated to the patellar sphere ratio (ICC 0.60, P = .05). FIGURE 6 Fitted spheres for the patella and distal femoral condyles (yellow) in the mediolateral (xy) plane. Spheres were fitted to the central strip of the left patella (green) and femoral trochlea 4 | DISCUSSION (red). The red lines define the extent of the arc length, with the resultant angle between the lines defined as theta. The defined points represent the centre point of the spheres fitted to the This study demonstrates that distal femoral and proximal tibial epi- articular surfaces. The y‐axis represents the vertical axis, with the physiodesis alters the limb length ratios and subsequent patellar x‐axis representing the horizontal axis of the coordinate system as height in a skeletally immature rabbit cohort. Compared with the defined [Color figure can be viewed at wileyonlinelibrary.com] control group, relative patella baja and a shorter femur (group FE)

 DAN ET AL. | 7

FIGURE 7 Articular surfaces for the trochlea, patella, medial and lateral tibial plateaus in the anterior (yz) plane. The Caton‐Deschamps measurement for patella height was taken as the distance between the midpoint of the tibial plateau to the inferior pole of the patella. The Insall‐Salvati measurement was taken as the distance between the centre of the tibial patella tendon insertion (red) and the centre of the patella articular surface (solid black line). The patella‐ trochlea engagement measurement was defined as the distance between the centre of the patella articular surface and most superior point of the femoral trochlea articular surface (dashed line). The patella tendon length (dot‐dashed black line) was measured as the inferior pole of the patella to the centre of the patella tendon insertion on the tibia (red) [Color figure can be viewed at wileyonlinelibrary.com]

FIGURE 8 A, Separation of medial and lateral aspects of the patella articular surface using a modified watershed algorithm (watershed line shown by larger points). B, Medial (red) and lateral (green) planes were fitted to the respective aspects of the patella articular surface. Normal vectors for these respective planes are represented by the gray arrows [Color figure can be viewed at wileyonlinelibrary.com]

 8 | DAN ET AL.

TABLE 1 Descriptive statistics for post hoc Tukey's HSD multiple comparison tests for multiple parameters between treatment groups

Treatment group

Control (C) Femoral epiphysiodesis (FE) Tibial epiphysiodesis (TE)

Mean (SD) Mean (SD) P value Mean (SD) P value

Femur length (mm) 85.51 (3.03) 75.65 (4.48) <.001a 86.04 (2.82) .91a <.001b

Tibia length (mm) 105.02 (3.78) 104.88 (2.39) .99a 94.49 (4.13) <.001a <.001b

Limb length (femur:tibia) 0.81 (0.01) 0.72 (0.04) <.001a 0.91 (0.04) <.001a ratio <.001b

Patellar tendon 19.36 (0.96) 17.31 (1.79) .001a 18.36 (1.40) .15a length (mm) .11b

9.43 (2.84) 3.17 (4.66) <.001a 6.00 (4.31) .06a .13b

Insall‐Salvati Index 20.13 (2.04) 18.07 (2.79) .001a 19.53 (1.73) .06a .18b

Modified Caton‐ 20.87 (1.76) 18.89 (1.06) .04a 22.81 (2.18) .02a Deschamps Index <.001b

Patella to femoral 9.64 (2.73) 7.45 (2.19) .10a 7.33 (3.52) .08a trochlea distance .99b

Angle between medial/ 53.40 (5.43) 51.88 (10.08) .85a 51.42 (6.52) .76a lateral articular .99b surfaces Sagittal patella articular 9.35 (0.55) 9.24 (0.89) .90a 9.50 (0.61) .84a glide length .56b

Patella theta 8.18 (2.19) 21.11 (5.28) .15a 12.69 (3.17) .52a .69b

Sagittal patella sphere 10.69 (1.16) 13.19 (5.86) .16a 11.13 (1.44) .94a radius .25b

Femoral trochlea 21.48 (2.18) 16.47 (3.13) <.001a 21.26 (4.02) .98a articular glide length <.001b

Femoral trochlea theta 89.44 (8.18) 74.71 (21.11) .030a 85.13 (12.69) .721a .141b

Trochlea sphere radius 14.82 (1.72) 14.08 (3.83) .742a 15.22 (2.15) .920a .479b

Difference in the trochlea 4.98 (2.21) 0.68 (3.50) .002a 5.47 (3.67) .91a and patella centre <.001b point of rotation Knee flexion angle 44.38 (13.72) 45.06 (11.48) .99a 34.09 (15.06) .11a .07b

Note: Significant values are highlighted in bold. aCompared to group C. bCompared to group FE.

and relative patella alta and a shorter tibia (group TE), was induced to patellar tendon force ratio with changing degrees of knee by epiphysiodesis. flexion,25 and (c) increase the moment arm of the knee.26 Patella In evolutionary science, it is widely accepted that function alta is associated with decreased joint contact area,27 subsequent dictates anatomy.23 The function of the patella is to (a) decrease the increased patellofemoral contact forces28 and the development of coefficient of friction between the extensor mechanism and the patellofemoral arthritis.29 Patella alta is also widely recognized to trochlea,24 (b) act as a lever to alter the relative quadriceps tendon increase the efficacy of the extensor mechanism due to the greater

 DAN ET AL. | 9

the knee to bodyweight axis with a longer femur (tibial epiphy- siodesis) and a decreased distance from the knee to the bodyweight axis with a short femur (femoral epiphysiodesis). Given that the torque on either side of the knee needs to balance for a joint to be in equilibrium, if the distance from the knee to the axis of the bodyweight is increased, the force required to balance this torque at the knee is also increased. If the muscular force generated is constant, the only way to increase the torque of the extensor me- chanism is to increase the moment arm. The moment arm function of the patella seems to dictate the sagittal patellofemoral anato- mical height; however, given we could not precisely control knee flexionangle,wewereunabletoconfirmthisbymeasuringthe distance between the patella and femoral epicondyles, as with in- creasing knee flexion there is increased patella engagement within the trochlea/translation distally which will affect this measurement. Therefore we make the inference from the work of Ward et al30 where patella alta has been shown to increase the moment arm and FIGURE 9 3D model representation of limb length ratios and extensor mechanism efficacy. modified Caton‐Deschamps measurements for groups C, FE and TE. 3D, 31 three‐dimensional; Group FE: relatively short femur/long tibia with Patella height and trochlea curve are interrelated. In our study, patellar baja; Group TE, relatively long femur/short tibia with patellar alta we demonstrated that the sagittal curvature of the patella height was [Color figure can be viewed at wileyonlinelibrary.com] related to the trochlea's radius of curvature. As patella height in- creased, a shorter, more curved trochlea developed. This finding moment arm of the patella in knee extension compared with knee suggests that the patella's maximal moment arm associated with flexion.30 knee extension is maintained for longer in moving from extension to In our study, distal femoral and proximal tibial epiphysiodesis flexion before the necessary trochlea depth relative to the condyles changed the relative limb length ratio and therefore, the relative develops to allow for terminal knee flexion with a relatively longer sagittal balance of the hindlimb. There is an increased distance from femur (Figure 10). Additionally, given that the distal femoral physis

FIGURE 10 A, Femoral epiphysiodesis (FE), B, control (C), and C, tibial epiphysiodesis (TE) treatment group representative samples. Femoral condyles (yellow), fitted spheres (purple, centre of rotation shown by the dark purple point in the spheres), femoral trochlea (red) and patella (green) are shown for all treatment groups. Viewpoints are aligned with the calculated femoral condyle axis of rotation (defined by the vector between medial and lateral condyle fitted sphere centre points). A, Group FE: shorter trochlea, less curved than B the Control group, centre point of rotation for the femoral trochlea surface closer to the patella compared to B control group. B, Control Group: The patella radius of curvature is less than the femoral trochlea radius of curvature. Centre points of rotation for the patella and trochlea surfaces are not coincidental, nor close to one another. C, Group TE: Larger radius of curvature and shorter trochlea than B group C [Color figure can be viewed at wileyonlinelibrary.com]

 10 | DAN ET AL. contributes directly to trochlear development,12 a shallow trochlear ORCID depth may be explained by distal femoral physeal closure. Michael J. Dan http://orcid.org/0000-0002-3193-8048 Limb length ratios are meant to be constant; a tibia to femur Rema A. Oliver http://orcid.org/0000-0002-2381-7326 ratio of 0.8.32 Human cadaveric data suggests that increasing this William R. Walsh http://orcid.org/0000-0002-5023-6148 ratio (longer tibia) predisposes an individual to hip and knee arthritis.33 The clinical relevance of altered limb length ratios is REFERENCES otherwise largely not appreciated. This study opens pandoras box 1. Hall‐Craggs ECB. The effect of experimental epiphysiodesis on to investigate the association between limb length ratios and growth in length of the rabbit's tibia. J Bone Joint Surg Br. 1968;50(2): 392‐400. patellar height and subsequent dislocation in humans. Long- 2. Tanaka MJ. Editorial commentary: which came first, the patella or the itudinal studies are indicated to determine if patella alta is as- trochlea? Morphological relationships in patients with patellar in- sociated with premature physeal closure and/or a developmental stability. Arthroscopy. 2018;34(6):1929‐1930. response to a weaker quadriceps mechanism. Additionally, 3. Vries B. Zur Anatomie der Patella. Vehr. Anat. Ges Anat An., Ergän- zungsh Z Bd. 1908;32:163‐169. potential early surgical interventions for skeletally immature 4. Gray D, Gardner E. Prenatal development of the human knee and patients with patellar alta and trochlea dysplasia requires superior tibiofibular joints. Am J Anat. 1950;86(2):235‐287. further study. 5. Doskocil M. Formation of the femoropatellar part of the human knee Our study was limited given we were unable to perform shape joint. Folia Morphol. 1985;33(1):38‐47. analysis to reflect trochlea dysplasia; however, this has been well 6. Weinstein SL. Natural history of congenital hip dislocation (CDH) and hip dysplasia. Clin Orthop Relat Res. 1987;225:62‐76. documented in previous human and animal‐based studies.7,12 The 7. Li W, Wang Q, Wang F, Zhang Y, Ma L, Dong J. Femoral trochlear role of the anterior femoral physis in the development of trochlear dysplasia after patellar dislocation in rabbits. Knee. 2013;20(6): dysplasia has been previously explored.12 It was outside the scope of 485‐489. our study to investigate this; however, further investigation is war- 8. Wang S, Ji G, Yang X, et al. Femoral trochlear groove development after patellar subluxation and early reduction in growing rabbits. Knee ranted to explore the value of selective femoral epiphysiodesis in the Surg Sports Traumatol Arthrosc. 2016;24(1):247‐253. 12 treatment of trochlea dysplasia for skeletally immature patients. 9. Huri G, Atay OA, Ergen B, Atesok K, Johnson DL, Doral MN. Devel- The tibial apophysis was also not ablated in our study and therefore, opment of femoral trochlear groove in growing rabbit after patellar ‐ the effect of tibial apophyseal closure on patellar height could not be instability. Knee Surg Sports Traumatol Arthrosc. 2012;20(2):232 238. 10. Kaymaz B, Atay OA, Ergen FB, et al. Development of the femoral assessed. trochlear groove in rabbits with patellar malposition. Knee Surg Sports Traumatol Arthrosc. 2013;21(8):1841‐1848. 11. Nietosvaara Y. The femoral sulcus in children. An ultrasonographic 5 | CONCLUSION study. J Bone Joint Surg Br. 1994;76(5):807‐809. 12. Parikh SN, Rajdev N, Sun Q. The growth of trochlear dysplasia during adolescence. J Pediatr Orthop. 2018;38(6):e318‐e324. Distal femoral and proximal tibial epiphysiodesis altered the relative 13. Waterman BR, Belmont PJ, Owens BD. Patellar dislocation in the limb length ratio of the hindlimb in this experimental rabbit model. The United States: role of sex, age, race, and athletic participation. J Knee associated limb length ratios lead to developmental differences in Surg. 2012;25(01):051‐058. 14. Sanders TL, Pareek A, Hewett TE, Stuart MJ, Dahm DL, Krych AJ. patellar height with associated morphological changes to the curva- Incidence of first‐time lateral patellar dislocation: a 21‐year ture of the trochlea whilst patella morphology remained unchanged. population‐based study. Sports Health. 2018;10(2):146‐151. Our findings suggest anatomical development of the patellofemoral 15. Harcke HT, Synder M, Caro PA, Bowen JR. Growth plate of the joint is dictated by moment arm function and is potentially responsible normal knee: evaluation with MR imaging. Radiology. 1992;183(1): ‐ for the etiology of patella alta. Future studies are warranted to explore 119 123. 16. Hall‐Craggs EC, Lawrence CA. The effect of epiphysial stapling on this association further with the view for the development of treat- growth in length of the rabbits tibia and femur. J Bone Joint Surg Br. ment options for patella alta in human patients. 1969;51(2):359‐365. 17. Wu G, Siegler S, Allard P, et al. ISB recommendation on definitions of ACKNOWLEDGMENTS joint coordinate system of various joints for the reporting of human joint motion—part I: ankle, hip, and spine. J Biomech. 2002;35(4): All authors have no conflict of interest. All authors do not have any 543‐548. interest or relationship, financial or otherwise, that might be per- 18. Parr WCH, Chatterjee HJ, Soligo C. Calculating the axes of rotation ceived as influencing an author's objectivity. for the subtalar and talocrural joints using 3D bone reconstructions. J Biomech. 2012;45(6):1103‐1107. 19. Parr WCH, Soligo C, Smaers J, et al. Three‐dimensional shape varia- AUTHOR CONTRIBUTIONS tion of talar surface morphology in hominoid primates. J Anat. 2014; All authors have made substantial contributions to research design, 225(1):42‐59. or the acquisition, analysis or interpretation of data; drafting the 20. Caton J, Deschamps G, Chambat P, Lerat JL, Dejour H. [Patella infera. paper or revising it critically; approval of the submitted and final Apropos of 128 cases]. Rev Chir Orthop Reparatrice Appar Mot. 1982; 68(5):317‐325. versions. All authors have read and approved the final submitted 21. Insall J, Salvati E. Patella position in the normal knee joint. Radiology. manuscript. 1971;101(1):101‐104.

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22. Dejour D, Ferrua P, Ntagiopoulos PG, et al. The introduction of a new 32. Strecker W, Keppler P, Gebhard F, Kinzl L. Length and torsion of the MRI index to evaluate sagittal patellofemoral engagement. Orthop lower limb. J Bone Joint Surg Br. 1997;79(6):1019‐1023. Traumatol Surg Res. 2013;99(8 Suppl):S391‐S398. 33. Weinberg DS, Liu RW. The association of tibia femur ratio and de- 23. Moss ML, Young RW. A functional approach to craniology. Am J Phys generative disease of the spine, hips, and knees. J Pediatr Orthop. Anthropol. 1960;18(4):281‐292. 2017;37(5):317‐322. 24. Hungerford DS, Barry M. Biomechanics of the patellofemoral joint. 34. Dejour H, Walch G, Nove‐Josserand L, Guier C. Factors of patellar Clin Orthop Relat Res. 1979;144:9‐15. instability: an anatomic radiographic study. Knee Surg Sports Traumatol 25. Huberti HH, Hayes WC, Stone JL, Shybut GT. Force ratios in the quad- Arthrosc. 1994;2(1):19‐26. riceps tendon and ligamentum patellae. JOrthopRes. 1984;2(1):49‐54. 26. Kaufer H. Mechanical function of the patella. J Bone Joint Surg Am. 1971;53(8):1551‐1560. SUPPORTING INFORMATION 27. Ward SR, Terk MR, Powers CM. Patella alta: association with pa- Additional supporting information may be found online in the ‐ tellofemoral alignment and changes in contact area during weight Supporting Information section. bearing. J Bone Joint Surg Am. 2007;89(8):1749‐1755. 28. Ward SR, Powers CM. The influence of patella alta on patellofemoral joint stress during normal and fast walking. Clin Biomech. 2004;19(10): 1040‐1047. How to cite this article: J Dan M, Parr WC, Crowley JD, et al. 29. Stefanik JJ, Zhu Y, Zumwalt AC, et al. Association between patella alta and the prevalence and worsening of structural features of patello- Moment arm function dictates patella sagittal height femoral joint osteoarthritis: the multicenter osteoarthritis study. anatomy: Rabbit epiphysiodesis model alters limb length Arthritis Care Res. 2010;62(9):1258‐1265. ratios and subsequent patellofemoral anatomical 30. Ward SR, Terk MR, Powers CM. Influence of patella alta on knee development. J Orthop Res. 2020;1–11. extensor mechanics. J Biomech. 2005;38(12):2415‐2422. https://doi.org/10.1002/jor.24714 31. Ferlic PW, Runer A, Dammerer D, Wansch J, Hackl W, Liebensteiner MC. Patella height correlates with trochlear dysplasia: a computed tomography image analysis. Arthroscopy. 2018;34(6):1921‐1928.

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 The Knee 26 (2019) 115–123

Contents lists available at ScienceDirect

The Knee

Patella tendinopathy Zoobiquity — What can we learn from dogs?☆

Michael J. Dan a,⁎,JamesCrowleya, David Broe a, Mervyn Cross b, Chris Tan a, William R. Walsh a a The Surgical and Orthopaedic Research Laboratory, Prince of Wales Clinical School University of NSW, Randwick, NSW, Australia b The Stadium Sports Clinic, Sydney, Australia article info abstract

Article history: Background: Patella tendinopathy is an overuse condition. Pathogenesis and identification of Received 10 September 2018 intrinsic risk factors have largely eluded the orthopaedic world. The cranial cruciate ligament Received in revised form 30 October 2018 (CrCL) in dogs is the equivalent to the human anterior cruciate ligament (ACL). We report Accepted 10 November 2018 the effect of two canine proximal tibial osteotomy procedures in the veterinary literature on patella tendon moment arm and describe the biomechanical rationale for a tibial tubercle osteotomy for treatment of patella tendinopathy in the human. Methods: A literature review of studies reporting clinical complications of TTA and TPLO to form an observational animal cohort study in dogs. Results: The veterinary literature reports an overall clinical complication rate of up to 61% for TTA and up to 50% for TPLO respectively. Complications associated with the extensor mecha- nism of the knee are b1% for TTA compared to 1.9–19% for TPLO. Radiographic thickening of the patella tendon and tendinopathy is seen in one to 80% of TPLO cases. The TPLO decreases the moment arm of the extensor mechanism meaning increased force is required in the patella tendon to achieve the same torque when compared to the TTA which increases the efficiency of the extensor mechanism. This difference may account, in part, for the post-operative compli- cations reported to the patella and patella tendon following TPLO. Conclusion: This observational animal cohort study demonstrates a biomechanical rationale for investigating diagnostic and potential treatment options, including a tibial tubercle osteotomy, for patella tendinopathy in humans based on this principle. © 2018 Elsevier B.V. All rights reserved.

1. Introduction

Patella tendinopathy is an overuse condition most commonly affecting jumping athletes, with a reported incidence of greater than 50% for volleyball and basketball players and an overall incidence of 14% [1]. Patella tendinopathy is characterised by pain and tenderness at the distal pole of the patella [2]. There is a 53% incidence of retirement due to patella tendinopathy vs seven percent of other athletes retiring due to injury [3]. Risk factors for the condition are either extrinsic that are external to the athlete or intrinsic which are internal to the athlete. Extrinsic risk factors include increased training volume and harder training surfaces [4–6]. Intrinsic risk factors include hamstring and muscle tightness [7], abnormal leg lengths and loss of medial arch of the foot [5]. Previous studies have failed to show a sta- tistical difference in the morphology of the patella of those with and without patella tendinopathy [8,9,4]. These studies have ex-

☆ Declarations of interest: none. ⁎ Corresponding author at: Surgical & Orthopaedic Research Laboratories, Prince of Wales Hospital, Level 1, Clinical Sciences Building, Randwick, NSW 2031, Australia. E-mail address: [email protected] (M.J. Dan).

https://doi.org/10.1016/j.knee.2018.11.010 0968-0160/© 2018 Elsevier B.V. All rights reserved.

 116 M.J. Dan et al. / The Knee 26 (2019) 115–123 amined the patella for differences in anatomy based on radiographic risk factors associated with patellofemoral pain and disloca- tion. Kujala et al. [10] found differences in the patella height of those with patella tendinopathy and Tscholl et al. [11] again found differences regarding patella height, tilt and tibial tubercle trochlea groove distance. However these mean differences were still largely within the range of quoted normal values for these measures, suggesting we need to redefine how we view abnormalities of the extensor mechanism related to patella tendinopathy. There are a multitude of treatments for patella tendinopathy [12]. Surgery is performed on the premise of replacing a ‘bad scar’ with ‘good scar’ [13]. There is no proven benefit to surgery with high level evidence [14]. Multiple treatments combined with on- going patient morbidity reflects that none of these treatments are truly effective. We have proposed that the answer to identifying patella based intrinsic risk factors and improving treatment lies in addressing the biomechanics of the extensor mechanism through a tibial tubercle osteotomy [15]. The patella's role in the extensor mecha- nism is to increase the moment arm of the knee [16] and act as a lever to change the patella and quadriceps force vector through flexion [17]. We have demonstrated differences in the patella's lever arm in a radiographic case control series in those with patella tendinopathy compared to normal subjects [18]. Animal models for patella tendinopathy are not inducive to exploring these biomechanical risk factors and treatment. Animal models for patella tendinopathy can be induced mechanically by repetitive loading causing micro trauma to the tendon or chem- ically by collagenase injection. These models are limited in that the condition can self-resolve and they are performed in small animals with significant gait differences to humans, namely walking or hoping with a flexed knee [19,20,21]. Zoobiquity is the term used to describe the collaboration between the human and veterinary professions in order advance sci- entific understanding in both fields [22]. Zoobiquity is based on the assumption that humans and animals share commonalities with respect to the pathogenesis of disease; synonymous with the One Health Initiative [23]. It's role in orthopaedics and dogs has recently been explored with hip dysplasia [24]. The cranial cruciate ligament (CrCL) is the canine equivalent of the human anterior cruciate ligament (ACL). CrCL rupture is one of the most common causes of lameness in dogs [25]. Surgical intervention is preferred over conservative management to re-establish joint stability, mitigate secondary degenerative joint disease, and address any concurrent meniscal injury [26,27].Al- though debate continues over which is better, tibial plateau levelling osteotomy (TPLO) and tibial tuberosity advancement (TTA) are two commonly performed proximal tibial osteotomies that stabilise the CrCL deficient stifle joint by neutralising tibiofemoral shear forces [28]. Patella tendinopathy (also known as tendinitis or desmitis in the veterinary literature) is a rare clinical form of lameness on its own in dogs, but is commonly reported post-operatively following TPLO [29,30]. Comparatively, TTA is typically not associated with patella tendinopathy [28]. In this paper, our aim was to explore the complications following the TPLO and TTA procedures in dogs, summarising these complications in relation to development of patella tendinopathy. In the discussion we will explore the biomechanical principles of the knee joint, specifically the patella tendon. In addition, we describe the relevance of such knowledge in the management and treatment of patella tendinopathy in humans.

2. Methods

A literature review was performed with PubMed using MeSH terms “dog” AND “cranial cruciate” AND “osteotomy” AND “com- plication” which generated 123 results. We screened abstracts and full texts and included studies which related to TTA and/or TPLO and included a quantitative description of the complications of each group. A total of 28 studies were found and grouped by the osteotomy type to allow for an observational cohort study based on the osteotomy for comparison of complications. We grouped studies which reported on both clinical and radiographic patella tendinopathy to provide a non-weighted group summary of studies that reported on extensor mechanism complications. The studies included were of low level evidence, as such no meta-analysis was performed [31]. Patella tendinopathy was defined as reported by the authors, clinically or radiologically, using the terms ‘tendinopathy’, ‘ten- dinitis’ or ‘desmitis’.

3. Results

Tables 1 and 2 list the 28 studies obtained following literature review. Studies are described by study design, number of pro- cedures, mean dog age and weight with standard deviation when reported. The majority of studies are retrospective, involve me- dium to large breed dogs aged between four and six years of age. Tables 3 and 4 provide an individual breakdown of the complications reported for both procedures. There was an overall com- plication rate of and 7.2–50% and 11.3–34% for TTA and TPLO respectively. Where cells are left blank it means the paper did not specifically report that complication. Table 5 provides a non-weighted group summary of studies that reported on both clinical and radiographic patella tendinopathy. Patella tendinopathy is rarely reported following TTA but has a radiographic incidence of 19%, associated lameness of 5.9% and tendon rupture or patella fracture of 10.7% following TPLO. We considered tibial tuberosity fracture to be a complica- tion relating directly to the osteotomy of the TTA and not altered biomechanics so it was not included in Table 5.

 M.J. Dan et al. / The Knee 26 (2019) 115–123 117

Table 1 Summary of retrospective and prospective studies where standard and modified tibial tuberosity advancement (TTA) was performed.

Study Study design Number of procedures Age (years) Body weight (kg)

Hoffmann et al., 2006 [32] Retrospective 65 5.2 ± 2.5 39.7 ± 11.9 Stein & Schmoekel, 2008 [33] Retrospective 70 4.6 N/A Steinberg et al., 2011 [34] Retrospective 193 5.5 38.5 Hirshenson et al., 2012 [35] Retrospective 101 4.5 39.1 Wolf et al., 2012 [36] Retrospective 501 5.44 34.4 Christopher & Cook, 2013 [37] Retrospective 18 5.05 40.2 Pettit et al., 2014 [38] Prospective 25 4.7 36.8 Ramirez et al., 2015 [39] Retrospective 84 5.1 ± 2.6 28 ± 13 Butterworth et al., 2017 [40] Retrospective 152 5.96 27.7 Lafaver et al., 2007 [41] Retrospective 114 5.9 36.7 Ferreira et al., 2016 [42] Prospective 12 4.8 ± 1.9 35.5 ± 8.5 DeSandre-Robinson et al., 2017 [43] Retrospective 47 5.6 ± 2.6 33.0 ± 7.8 Hans et al., 2017 [44] Retrospective 91 5.0 ± 2.2 55.4 Lefebvre et al., 2018 [45] Retrospective 174 6 28.8

Age and weight of dogs in these studies are reported as mean ± standard deviation (SD).

4. Discussion

4.1. Clinical aspects in dogs

Patella tendinopathy in dogs is largely observed as thickening of the patella tendon on imaging modalities such as radiography and ultrasound [29]. Radiographic findings include thickening of the distal patella tendon, as opposed to the proximal part of the tendon in humans, demonstrated in Figure 1. Ultrasound findings are similar to the human with thickening and heterogeneity of the echogenicity of the tendon. Clinical lameness due to patella tendinopathy is much less than the incidence of tendon thickening on radiography [29]. This lameness largely resolves with time or physiotherapy but occasionally results in patella tendon rupture or patella fracture. There is emerging literature from Pettit et al. [38] and DeSandre-Robinson et al. [43] of an increasing incidence of patella ten- don thickening with TTA. These studies are in contrast to the majority of the reported literature as outlined in Table 3.Noasso- ciated clinical problems with the extensor mechanism have been noted. Therefore, it remains that patella tendinopathy is not associated with TTA.

4.2. Aetiology

While some studies suggest the difference in extensor mechanism related complications between TTA and TPLO could be at- tributed to non-biomechanical factors, these are hard to support. Pacchiana et al. [47] and Carey et al. [30] propose that patella tendinopathy may be due to differences in the post operative activity of dogs and/or intra-operative disruption to the blood sup- ply of the patella tendon. It is difficult if not impossible to standardise post operative activity in this animal cohort or enforce strict owner compliance. We do not see how post-operative activity levels could be attributed to complications of the procedure itself.

Table 2 Summary of studies where tibial plateau levelling osteotomy (TPLO) was performed.

Study Study design Number of procedures Age (years) Body weight (kg)

Barnhart et al., 2003 [46] Retrospective 25 4.9 36.1 Pacchiana et al., 2003 [47] Retrospective 397 5.0 ± 0.1 39.9 ± 0.6 Priddy et al., 2003 [48] Retrospective 253 4.7 ± 2.1 41.2 ± 11.7 Carey et al., 2005 [30] Retrospective 94 5 ± 2.5 36.8 ± 11.5 Stauffer et al., 2006 [49] Retrospective 696 6.2 38.4 Corr et al., 2007 [50] Retrospective 21 3.9 ± 1.8 47.9 ± 16.5 Conkling et al., 2010 [51] Prospective 118 5.7 41.7 Cook et al., 2010 [52] Prospective 23 5.7 ± 2.5 38.8 ± 16.3 Fitzpatrick & Solano, 2010 [53] Retrospective 1146 5.6 32 Gatineau et al., 2011 [54] Retrospective 476 5 36 Christopher & Cook 2013 [37] Retrospective 65 4.76 38.4 Coletti et al., 2014 [55] Retrospective 1519 5.4 ± 2.6 37.3 ± 11.0 Witte et al., 2014 [56] Retrospective 29 5.4 ± 2.7 9.2 ± 2.5 Barnes et al., 2016 [57] Retrospective 26 7 10.3 Ferreira et al., 2016 [42] Retrospective 15 4.4 ± 1.9 34.9 ± 11.1 DeSandre-Robinson et al. 2017 [43] Retrospective 59 4.4 ± 2.3 33.1 ± 10.9 Hans et al., 2017 [44] Retrospective 54 4.4 ± 2.3 59.6 Knight & Danielski, 2018 [58] Retrospective 66 6.4 ± 2.7 9.5 ± 1.9

Age and weight of dogs in these studies are reported as mean ± standard deviation (SD).

 118

Table 3 Summary of postoperative complications reported in prospective and retrospective studies following tibial tuberosity advancement (TTA) in dogs.

Hoffmann Lafaver et Stein & Steinberg Hirshenson Wolf et al., Christopher Pettit et al., Ferreira et Ramirez et Butterworth DeSandre-Robinson Hans et al., Lefebvre et al., al., 2007 Schmoekel, et al., et al., 2012 [36] & Cook, 2014 [38] al., 2016 al., 2016 et al., et al., 2017 [43] 2017 [44] et al., 2006 [32] [41] 2008 [33] 2011 [34] 2012 [35] 2013 [37] [42] [39] 2017 [40] 2013

Number of 65 114 70 193 101 501 18 25 12 84 152 47 91 174 procedures Surgical wounda 19 7 2 5 6 33 4 2 2 8 Infection 3 1 1 1 14 Intraoperativeb 2 3 2 1 26 3 70 Implantsc 13 21 10 1 1 Repeat surgery 10 33 performed

Medial patella 115 (2019) 26 Knee The / al. et Dan M.J. 11 11 luxation Delayed union/non-- union Medial meniscal 37 6 105195 3 injury Stifle instability/- 2 pivot shift Fibula head fracture Other/not 8426 classified – 123

Extensor mechanism complications Patella tendon 1 2 12 43 1 thickening Patella 1 tendonitis Patella fracture Patella tendon rupture Tibial tuberosity 4 3 2 2 21 1 8 21 fracture Total number of 26 (27) 36 (36) 23 (12) 21 (21) 20 (20) 120 (95) 11 (11) 12 3 40 (43) 3 (11) 43 (43) 32 (31) 91 complications

Note discrepancy in total complications that we tallied from the listed individual complications compared with the cumulative total reported by authors in brackets. a Surgical wound complications include; wound dehiscence, seroma formation etc. b Intraoperative complications include; haemorrhage, broken drill bit, damage to medial tibial cortex, intra-articular screw placement etc. c Implant complications include; screw/plate/Kirshner wire loosening, breakage, failure etc.

 Table 4 Summary of postoperative complications reported in prospective and retrospective studies following standard tibial plateau levelling osteotomy (TPLO) in dogs.

Barnhart Pacchiana Priddy Carey Stauffer Corr et Conkling Cook Fitzpatrick Gatineau Christopher Coletti Witte Barnes Ferreira DeSandre-Robinson Hans Knight & et al., et al., et al., et al., et al., al., et al., et al., & Solano, et al., & Cook, et al., et al., et al., et al., et al., 2017 [43] et al., Danielski, 2003 2003 [47] 2003 2005 2006 2007 2010 2010 2010 [53] 2011 2013 [37] 2014 2014 2016 2016 2017 2018 [58] [46] [48] [30] [49] [50] [51] [52] [54] [55] [56] [57] [42] [44]

Number of 25 397 253 94 696 21 118 23 1146 476 65 1519 29 26 26 59 54 66 procedures Surgical wounda 517 5114410 6 47 1 99 Infection 10 25 3 1 1 66 14 9 1 14 Intraoperativeb 3236 3 Implantsc 66 6212411 3 2 Revision surgery 19 1 26 5 44 performed Medial patella 313 115 (2019) 26 Knee The / al. et Dan M.J. luxation Delayed union/non-- 63 union Medial meniscal 42 15610812 injury Stifle instability/- 14141 2 pivot shift Fibula head 952 12 1 2 fracture Other/not 316 721 4

classified – 123 Extensor mechanism complications Patella tendon 19 75 19 1 3 5 14 57 thickening Patella 2241 1 tendonitis Patella fracture 1 1 1 1 Patella tendon 4 rupture Tibial tuberosity 14 6 4 28 1 2 5 53 fracture 27 Total number of 95 (136) 35 131 10 (9) 184 15 5 (5) 106 16 (22) 9 (9) 258 (148) 57 (57) 15 (18) 4 (4) 557 (27) 15 (15) complications 23.92% (66) (131) 47.62% (173) (26) 50%

Note discrepancy in total complications that we tallied from the listed individual complications compared with the cumulative total reported by authors in brackets. a Surgical wound complications include; wound dehiscence, seroma formation etc. b Intraoperative complications include; haemorrhage, broken drill bit, damage to medial tibial cortex, intra-articular screw placement etc. c Implant complications include; screw/plate/Kirshner wire loosening, breakage, failure etc. 119

 120 M.J. Dan et al. / The Knee 26 (2019) 115–123

Table 5 Complications of the extensor mechanism for tibial tuberosity advancement (TTA) and tibial plateau levelling osteotomy (TPLO) procedures.

Extensor mechanism complications TTA [41]a TPLO [47,48,30,49,52,53,57]a

Patella tendon thickening 1 (b1%) 94 (19%) Patella tendinitis (clinical) 1 (b1%) 29 (5.9%) Patella fracture 22 (1.9%) Patella tendon rupture 61 (8.8%)

a Only those studies that individually reported both radiographic thickening and clinical tendinopathy were included.

Further, Johnson et al. [59] examined the effect of TTA and TPLO cadaveric procedures on the blood supply to the patella tendon and found both procedures disrupt the same vasculature due the requirement for knee arthrotomy, however this does not pre- clude the possible aetiology of scarring associated with violation of the fat pad with the TPLO (Figure 2). Boudrieau [28] explored the biomechanical differences between TTA and TPLO. Torque is a rotational force that it is equal to the moment arm (perpendicular distance from the force vector to the point of rotation) multiplied by the force vector. In a TTA, the moment arm is increased. Therefore, to achieve the same extension torque, less force is required through the patella tendon. Conversely, TPLO which is the point of rotation on the femur is brought anterior relative to the tibia, which decreases the relative moment arm. Therefore, to achieve the same torque, a larger amount of force is exerted through the patella tendon. It is this in- creased force/load that may explain the higher incidence of patella tendinopathy following TPLO. Comparatively, TTA may have a protective effect on the patella tendon due to the decreased force exerted while maintaining the efficiency in torque. See Figure 1 for a visual demonstration of this concept. This concept is in agreeance with the human cadaveric work by Kaufer [16] and Maquet [60] which established the moment arm role of the patella and the utility of anteriorisation of the tibial tubercle. Lewallen et al. [61] also demonstrated a trend for the force through the patella tendon to decrease with anteriorisation of the patella tendon for 30–60 degrees of knee flexion. The veterinary literature is not consistent on patella tendon forces in CrCL deficient dogs following TPLO and TTA. Drew et al. [62] claimed to show no difference in the stifle extensor mechanism following TPLO of CrCL in-tact stifles of canine cadavers. However, they applied and measured the force at the patella (bone) and claimed it represented the patella tendon force. This as- sumes the extensor mechanism is a pulley, which is inaccurate as it fails to take into account the lever role of the patella with the changing patella tendon to quadriceps tendon force ratio based on the amount of knee flexion [17]. Comparatively another study has shown the TPLO does lower the force required to fracture the patella with an applied quadriceps load [63],supportingthe theory that the decreased moment arm of TPLO increases the forces through the extensor mechanism.

4.3. Relevance to humans

There are different aetiologies attributed to patella tendinopathy. We have explored this in greater detail previously [15], suf- fice to say we concede that there is debate over the aetiology of patella tendinopathy as a stress shielding/compressive phenom- enon [1,2] vs a repetitive micro-overload pathogenesis. There appears to be sufficient clinical evidence to exclude compressive aetiology [16] and ample biomechanical cadaveric evidence and finite element models to support repetitive micro-overload

Figure 1. Patella tendon thickening post TPLO. The radiograph on the left was taken immediately post-operatively showing the normal outline of the patella ten- don. The radiograph on the right was taken 6 weeks post-operatively and demonstrates thickening of the distal portion of the patella tendon (arrow).

 M.J. Dan et al. / The Knee 26 (2019) 115–123 121

Figure 2. Moment arm differences following tibial tuberosity advancement (TTA) and tibial plateau levelling osteotomy (TPLO). Following TTA, the moment arm (MA) is increased; therefore, to achieve the same extension torque, less force is required through the patella tendon (PT). Conversely, following TPLO, the point of rotation is changed and as a result the moment arm of the PT is shortened. Therefore, to achieve the same torque, a larger amount of force is exerted through the patella tendon. Note: differences in PT magnitude are reflected by font size. T = tibia, F = femur.

[3,8,12]. The repetitive micro-overload theory is in keeping with the known overload extrinsic risk factors from clinical studies [6,18,22]. Numerous papers have failed to identify patella based intrinsic risk factors as they have tried to associate known path- ological anatomies of patellofemoral pain and dislocation with tendinopathy, not biomechanical aspects of the extensor mecha- nism [8,9,4]. The patella has two roles; 1) as a lever and 2) to increase the moment arm of the extensor mechanism. We believe, in agreeance with Tscholl et al. [11], the answer to treating patella tendinopathy lies in altering the biomechanics of the extensor mechanism to be more favourable to the patella tendon [15]. Based on the work of Huberti et al. [17], identifying the patella as a lever in the sagittal plane, the patella tendon force is not 1:1 with the quadriceps tendon force. The ratio changes based on the lever arm generated due to whether the proximal or distal pole of the patella is articulating with the femur. We identified a shorter patella tendon lever arm as an intrinsic risk factor associated with the development of patella tendinopathy [18].This signifies that those with patella tendinopathy will experience greater force through their patella tendon compared to those with- out due to the relationship of their patella relative to the femur. A distalizing tibial tubercle osteotomy will alter the point of ar- ticulation of the patella on the femur, moving it proximally on the patella earlier in the knee flexion range. This change in the articulation point/pivot point/fulcrum of the patella will manipulate the patella tendon to quadriceps tendon force ratio to de- crease the force through the patella tendon and relatively increase the force through the quadriceps tendon earlier in the knee range of motion, the range associated with running, jumping and landing [64]. Previous study investigating moment arm characteristics as an intrinsic risk factor for patella tendinopathy in humans remain unreported. This animal model provides rationale for an anteriorising tibial tubercle osteotomy. As identified by Kaufer [16] and Maquet [60], by anteriorising the tibial tubercle the force required through the extensor mechanism to achieve the same amount of torque through the knee will be decreased. This offers a potential biomechanical solution to patella tendinopathy. Further biomechanical work is needed to quantify the effect of different tibial tubercle positions on the patella tendon forces and to ensure the patellofemoral articular forces are not substantially increased before implementing clinically.

5. Conclusion

This observational animal cohort study demonstrates the protective association of an increased patella tendon moment arm (TTA) and the detrimental effects of a decreased moment arm with the development of patella tendinopathy (TPLO) in dogs. This study supports the rationale for further clinical and cadaveric studies exploring the biomechanical and clinical outcomes of a tibial tubercle osteotomy as a biomechanical treatment for patella tendinopathy.

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 Novel treatment (new drug/intervention; established drug/procedure in new situation)

CASE REPORT BMJ Case Rep: first published as 10.1136/bcr-2019-229209 on 1 July 2019. Downloaded from Treatment of patella tendinopathy by distalising tibial tubercle osteotomy Michael J Dan, 1 William R Walsh,1 Mervyn J Cross,2 Bruce Caldwell3

1Prince of Wales Clinical School, SUMMARY !5 79,:,5;(;065 36>,9 304) (30.54,5; >(: University of New South Wales, Patella tendinopathy condition is often resistant to 5694(3 >0;/ ( 5694(3 +,.9,, 6- 9,*<9=(;<4 , Sydney, New South Wales, conservative treatment. We report a case of patella /(+05;(*;*633(;,9(330.(4,5;:5694(3*9<*0(;,30.( Australia 2 tendinopathy treated by distalisation of the tibial 4,5;:(5+56:0.5:6-4,50:*(37(;/636.@ Orthopaedics, Stadium Sports tubercle with excellent long-term result. %/, 7(;,33( >(: /0./ 05 76:0;065 (5+ ;9(*2,+ ( Clinic, Sydney, New South 30;;3, 3(;,9(33@ >0;/6<; ( :0.50-0*(5; :0.5 %/,9, Wales, Australia 3Orthopaedics, Lingard Private >(:56,--<:065(5+(-<339(5.,6-46;065 (92,+ ;,5+,95,::>(:56;,+(;;/,1<5*;0656-;/,7(;,33( Hospital, Merewether, New BACKGROUND ;,5+65(5+05-,9069763,6-;/,7(;,33( South Wales, Australia "(;,33(;,5+0567(;/@0:(56=,9<:,*65+0;0653(9.,3@ (--,*;05. /0./3,=,3 (;/3,;,: 05=63=,+ 05 1<4705. Correspondence to Dr Michael J Dan, :769;: %/, 469)0+0;@ 6- ;/0: *65+0;065 0: 6-;,5 INVESTIGATIONS michael. dan@ unsw. edu. au <5+,9,:;04(;,+ )@ 69;/67(,+0* :<9.,65: >0;/ ( #(+06.9(7/: :/6>,+ ( 5694(3 (;65,:*/(47: 9,;09,4,5;9(;,6- +<,;6;/,051<9@*647(9,+ 9(;06 6-   /6>,=,9 ( /0./ 5:(33$(3=(;0 9(;06 Accepted 29 May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http://casereports.bmj.com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on 4 July 2019 by guest. Protected copyright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© BMJ Publishing Group  Limited 2019. No commercial %/, 7(;0,5; /(+ /(+ ,?/(<:;0=, *65:,9=(;0=, (5+6/5:65 :,,-0.<9, 5+,,+/0:%%% re-use. See rights and 4,(:<9,:(;;/,05(5(;;,47;;6(=60+:<9.,9@!9(3 >(:5694(379,*3<+05.;/0:+0(.56:0: permissions. Published by BMJ. 4,+0*(;065: 05*3<+05. 7(9(*,;(463 (5+ 565:;, %/, (<;/69: +6 56; 9,(33@ ),30,=, ;/(; 6--(D: 960+(3 (5;005-3(44(;69@ 4,+0*(;065 >,9, <:,+ +0:,(:, (: ( 9,(3 +0:69+,9 ;/, :,5069 (<;/69: To cite: Dan MJ, Walsh WR, Cross MJ, et al. BMJ Case "/@:06;/,9(7@ 05=63=,+ 9,:; ,**,5;90* 36(+05. 4<:; /(=, 6**(:065(33@ ;9,(;,+ 0; )@ (9;/96:*670* Rep 2019;12:e229209. 796.9(44,:-3,?0)030;@,?,9*0:,:/(4:;905.;,5+65 +,)90+,4,5;6-;/,;076-;/,-(;7(+>/,50;/(: doi:10.1136/bcr-2019- :;9,;*/05.(5+69;/6;0*:;6*6<5;,9-66;7965(;065 ),,5:/6>5;6/(=,(5,?*,::0=,3@/0./:0.5(365 229209 %/,7(;0,5;+0+56;/(=,(*69;0*6:;,960+051,*;065 # :*(5 (5+ 56 6;/,9 +0(.56:,: (9, (77(9,5;

Dan MJ, et al. BMJ Case Rep 2019;12:e229209. doi:10.1136/bcr-2019-229209 1

 Novel treatment (new drug/intervention; established drug/procedure in new situation)

Surgical technique BMJ Case Rep: first published as 10.1136/bcr-2019-229209 on 1 July 2019. Downloaded from %/,7(;0,5;>(:73(*,+05(:<705,76:0;065>0;/(75,<4(;0* ;6<9508<,;(7730,+9;/96:*67@>(:7,9-694,+>0;/*65-094( ;0656-5694(3(9;0*<3(9:<9-(*,:%/,+0:;(3763,6-;/,7(;,33( >(:(9;/96:*670*(33@+,)90+,+%/,9,:;6-;/,25,,>(:5694(3  *405*0:065 >(: 4(+, *4()6=, ;/, 40+305, 65 ;/, 3(;,9(3 (:7,*; 6- ;/, +0:;(3 ;/0./ (5+ ( A0. A(. 0306;0)0(3 )(5+ 9,3,(:,-964(5;,9069;676:;,9069>(:7,9-694,+  *4365.0;<+05(3 05*0:065 >(: 4(+, 4,+0(3 ;6 ;/, ;0)0(3 Figure 1 Lateral radiographs from left to right are presented of ;<),9*3, %/, 7,906:;,<4 >(: ,3,=(;,+ 65 ;/, 4,+0(3 :0+,  the patient prior to surgery, immediately after surgery and at 3 and 6 ;0)0(3;<),9*3,6:;,6;64@>(:7,9-694,+(5+;/,;<),9*3,>(: months following surgery demonstrating union of the osteotomy of 46=,+ 444,+0(33@(5+ 44+0:;(33@%/0:>(:/,3+>0;/ reposition in the patella. ;>6*<;9(2 :*9,>: %/,7,906:;,<4>(:9,7(09,+;6;/,4,+0(3:0+,6-;/,:/05.3, #6<;05,*36:<9,>(:7,9-694,+ 05+05.:(;(9;/96:*67@-696--(D:+0:,(:,(9,=(.<,:@56=0;0: (5+(77,(930;;3,+0--,9,5;-9644(5@6;/,9-(;7(+:65,:,,:(; Postoperative management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

TREATMENT DISCUSSION <,;6-(03<9,6-*65:,9=(;0=,4,(:<9,::<9.,9@>(:6--,9,+ "(;,33(;,5+0567(;/@0:(56=,9<:,*65+0;06550;0(3;9,(;4,5;0: http://casereports.bmj.com/ ;@70*(33@*65:,9=(;0=,>0;/7/@:06;/,9(7@-3,?0)030;@(5+,**,5 ;90*36(+05.796.9(44,:)<;0;0:,:;04(;,+;/(; 6-7(;0,5;: >0;/7(;,33(;,5+0567(;/@>033*64,;6:<9.,9@;/6:,;@70*(33@ >0;/ .9(+,  69  :@47;64: )(:,+ 65 ;/, 3(A05( .9(+05. :@:;,4 6>,=,9 ;/, ),5,-0; 6- :<9.,9@ /(: ),,5 8<,:;065,+ )@ /0./3,=,3,=0+,5*,(5+0;0:9,(:65()3,;6:<..,:;;/(;:<9.,9@ 0:*<99,5;3@<;030:,++<,;6,?/(<:;0656-6;/,9;/,9(70,:9(;/,9 ;/(5+<,;60;:<;030;@ $64,,?7,9;:05-(*;/(=,46=,+(>(@-964:<9.0*(3+,)90+, on 4 July 2019 by guest. Protected copyright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igure 2 1.5-T MRI T2-weighted, sagittal plane of knee demonstrate 4,*/(50:4 )@ 05*9,(:05. ;/, 25,, 464,5; (94 $,*65+ the increased signal intensity intrasubstance and blurring of posterior (903@0;(*;:(:(3,=,905;/,:(.0;;(373(5,(3;,905.;/,7(;,33( superior tendon margin consistent with patella tendinopathy. ;,5+65 ;6 8<(+90*,7: ;,5+65 -69*, 9(;06 +,7,5+,5; 65 ;/,

2 Dan MJ, et al. BMJ Case Rep 2019;12:e229209. doi:10.1136/bcr-2019-229209

 Novel treatment (new drug/intervention; established drug/procedure in new situation)



-3,?065(5.3,6-;/,25,, %/,7(;,33(;,5+65-69*,(5+:;9(05 $6- -69;/6:,9,8<09,+:<9.,9@(5+>0;/($6--69 BMJ Case Rep: first published as 10.1136/bcr-2019-229209 on 1 July 2019. Downloaded from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ontributors MJD was involved in; conception and design, acquisition of data or ;/, 9(5., 6- 46;065 7(9;0*<3(93@ 05 ;/, 9(5., (::6*0(;,+ >0;/ analysis and interpretation of data, drafting the article and has given final approval  of the version submitted. He agrees to be accountable for the article and to ensure 9<5505.1<4705.(5+3(5+05. that all questions regarding the accuracy or integrity of the article are investigated %/,7(;0,5;9,769;,+(+0--,9,5*,6- (5+ 05/0:&$ and resolved. WRW was involved in editing of the article and concept design, and :*69, @,(9(5+@,(976:;:<9.,9@9,:7,*;0=,3@%/0:*647(9,: has given final approval of the version submitted. He agrees to be accountable for -(=6<9()3@>0;/;/,30;,9(;<9,.0=,59,769;,+=(3<,:6- >0;/( the article and to ensure that all questions regarding the accuracy or integrity of the article are investigated and resolved. MJC should be consider the forefather of this concept with large anecdotal experience not reported. He gave the senior surgeon the idea for the case. He was involved in editing of the article and concept design, and has given final approval of the version submitted. He agrees to be accountable Patient’s perspective for the article and to ensure that all questions regarding the accuracy or integrity of the article are investigated and resolved. BC was the surgeon assessing the patient and performing the case. He has reviewed the final version submitted and No one could diagnose me for ages until I saw (Senior surgeon), is accountable for the article to ensure that all questions regarding the accuracy or at which point I struggled to meet demands placed on my body integrity of the article are investigated and resolved. with rep (resentative soccer/football) training. The operation Funding The authors have not declared a specific grant for this research from any gave me the ability to continue football; however, I found it took funding agency in the public, commercial or not-for-profit sectors. over 6 months to get used to the change in my awareness of my

Competing interests None declared. http://casereports.bmj.com/ legs position in space, for example, I could not ride a skateboard Patient consent for publication Obtained. for the first 6 months although this was previously something I did with ease, this was not made aware to me and I think it is Provenance and peer review Not commissioned; externally peer reviewed. important to tell you. REFERENCES 1 Figueroa D, Figueroa F, Calvo R. Patellar Tendinopathy: Diagnosis and Treatment. J Am Acad Orthop Surg 2016;24:e184–92. Learning points 2 Dan M, Phillips A, Harris IA. Cochrane Musculoskeletal Group. Surgical interventions for patellar tendinopathy. Cochrane Database of Systematic Reviews 2018;88. Ź Patella tendinopathy is an overuse condition associated with 3 Bahr R, Fossan B, Løken S, et al. Surgical treatment compared with eccentric training for patellar tendinopathy (Jumper’s Knee). A randomized, controlled trial. J Bone Joint jumping related sports, which has an associated high rate of on 4 July 2019 by guest. Protected copyright. Surg Am 2006;88:1689–98. retirement and there is limited clinical benefit of traditional 4 Dan M, Parr W, Broe D, et al. Biomechanics of the knee extensor mechanism and its surgical excision in randomised control trials. relationship to patella tendinopathy: A review. J Orthop Res 2018;36:3105–12. Ź Extrinsic risk factors, those external to the athlete, are well 5 Tscholl PM, Biedert RM, Wanivenhaus F, et al. Patellar tendinopathy with proven and relate to sport type, training surface, training intratendinous alteration on MRI may be related to patellofemoral dysplasia. Scand J volume and duration. Med Sci Sports 2018;28:1443–50. 6 Warden SJ, Kiss ZS, Malara FA, et al. Comparative accuracy of magnetic resonance Ź Intrinsic risk factors, those internal to the athlete, have imaging and ultrasonography in confirming clinically diagnosed patellar tendinopathy. been proven to relate to Body Mass Index (BMI), leg length Am J Sports Med 2007;35:427–36. discrepancies, quadriceps and hamstring muscle tightness. 7 Johnson DP, Wakeley CJ, Watt I. Magnetic resonance imaging of patellar tendonitis. J Ź Intrinsic risk factors relating to an individual’s patellofemoral Bone Joint Surg Br 1996;78:452–7. 8 Ogon P, Maier D, Jaeger A, et al. Arthroscopic patellar release for the treatment of joint have historically not been proven, as investigators have chronic patellar tendinopathy. Arthroscopy 2006;22:462.e1–e5. tried to apply known anatomical anomalies associated with 9 Willberg L, Sunding K, Forssblad M, et al. Sclerosing polidocanol injections or patellofemoral instability and pain which fail to account for arthroscopic shaving to treat patellar tendinopathy/jumper’s knee? A randomised the biomechanical role of the extensor mechanism. controlled study. Br J Sports Med 2011;45:411–5. Ź This case demonstrates the potential clinical benefit of a 10 Blazina ME, Kerlan RK, Jobe FW, et al. Jumper’s knee. Orthop Clin North Am 1973;4:665–78. tibial tubercle osteotomy, which has the ability to manipulate 11 Roels J, Martens M, Mulier JC, et al. Patellar tendinitis (jumper’s knee). Am J Sports the sagittal position of the patella bone and consequently it's Med 1978;6:362–8. role as a lever in altering the relative quadriceps and patella 12 Ferretti A. Epidemiology of jumper’s knee. Sports Med 1986;3:289–95. tendon force ratios which warrants further clinical trials. 13 Insall J, Salvati E. Patella position in the normal knee joint. Radiology 1971;101:101–4.

Dan MJ, et al. BMJ Case Rep 2019;12:e229209. doi:10.1136/bcr-2019-229209 3

 Novel treatment (new drug/intervention; established drug/procedure in new situation)

14 Caton J, Deschamps G, Chambat P, et al. [Patella infera. Apropos of 128 cases]. Rev 19 Dan MJ, McMahon J, Parr WCH, et al. Evaluation of intrinsic biomechanical risk factors BMJ Case Rep: first published as 10.1136/bcr-2019-229209 on 1 July 2019. Downloaded from Chir Orthop Reparatrice Appar Mot 1982;68:317–25. in patellar tendinopathy: a retrospective radiographic case-control series. Orthop J 15 Seil R, Müller B, Georg T, et al. Reliability and interobserver variability in radiological Sports Med 2018;6:232596711881603. patellar height ratios. Knee Surg Sports Traumatol Arthrosc 2000;8:231–6. 20 Visentini PJ, Khan KM, Cook JL, et al. The VISA score: An index of 16 Kaufer H. Mechanical function of the patella. J Bone Joint Surg Am severity of symptoms in patients with jumper’s knee (patellar tendinosis). J Sci 1971;53:1551–60. Med Sport 1998;1:22–8. 17 Huberti HH, Hayes WC, Stone JL, et al. Force ratios in the quadriceps tendon and 21 Palmer SH, Servant CT, Maguire J, et al. Surgical reconstruction of severe ligamentum patellae. J Orthop Res 1984;2:49–54. patellofemoral maltracking. Clin Orthop Relat Res 2004;419:144–8. 18 van Eijden TM, Kouwenhoven E, Verburg J, et al. A mathematical model of the patellofemoral joint. J Biomech 1986;19:219–29.

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4 Dan MJ, et al. BMJ Case Rep 2019;12:e229209. doi:10.1136/bcr-2019-229209

         

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