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Patellar Tendon Fiber Strains: Their Differential Responses to Quadriceps Tension

Basso, Oreste; Amis, Andrew, A.; Race, Amos; Johnson, David, P.

Clinical Orthopaedics and Related Research: July 2002 - Volume 400 - Issue - p 246-253
SECTION II ORIGINAL ARTICLES: Research
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This study tested the hypothesis that the posterior fibers of the patellar tendon are subjected to higher tensile strains than the anterior fibers in response to quadriceps tension. The quadriceps tendon was loaded to 1 kN in 10 human cadaver knees and the tensile strain was measured in the anterior and posterior fibers of the patellar tendon. The central third patellar tendon was divided into anterior and posterior halves which were tensile tested to failure. The mean strain at 1 kN load was 1.7% (90° flexion), 2.7% (60°), and 3.9% (10°) anteriorly, and 3.2% (90°) 4.6% (60°), and 4.9% (10°) posteriorly. Quadriceps loading caused significantly greater strains in the posterior fascicles between 60° and 90° knee flexion. The material properties in the anterior and posterior regions were similar, except that failure strain was significantly higher posteriorly. Thus the posterior fascicles are adapted to sustain significantly greater tensile strains before failing. This suggests that the higher overall levels of tensile strain in the posterior fibers are not sufficient to explain the clinical pattern of patellar tendonitis.

From the Biomechanics Section, Department of Mechanical Engineering, Imperial College, London, UK.

Investigation done at Imperial College, London, England.

Reprint requests to Andrew A. Amis, DSc (Eng), Biomechanics Section, Department of Mechanical Engineering, Imperial College, London SW7 2BX, (UK).

Received: November 28, 2000.

Revised: August 6, 2001.

Accepted: October 11, 2001.

Patellar tendonitis is an inflammatory condition of the patellar tendon that causes anterior knee pain in jumping athletes. 3 Clinical examination reveals tenderness at the proximal patellar tendon. 9 Microscopic tears, mucoid degeneration, and fibrinoid necrosis usually are localized in the proximal, central portion of the tendon, at its posterior aspect. 3,9,11 The pathogenesis of patellar tendonitis is debatable. 5 It traditionally is considered an overuse condition, caused by tensile overload, although posterior impingement by the distal apex of the patella has been suggested. 9 The reason why the lesions are localized within the posterior fibers is unknown. 9 The simplest hypothesis would be that this part of the tendon is subjected to higher strain than the anterior fibers, because its fibers are shorter, 2 yet undergo similar tensile elongation under load.

This expected behavior has not been verified and it is not known how significant such a difference in strain might be. It also could be hypothesized that the cause of the selective damage seen in patellar tendonitis is a lower resistance to strain of the posterior fibers. The purpose of this investigation was to test these hypotheses by quantifying the strain in the anterior and posterior fibers of the patellar tendon caused by loading the knee extensor mechanism, and by measuring the material properties of the anterior and posterior fibers.

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MATERIALS AND METHODS

Specimen Preparation

Ten knees were harvested within 2 days of death from human cadavers (Table 1). The joints were removed by cutting the femur 150 mm proximal and the tibia 100 mm distal to the joint line. The knees were stored, with intact soft tissues, in sealed polyethylene bags at –20°C and thawed before dissection. Muscle tissue was removed; however, the capsule, ligaments, and approximately 150 mm of the quadriceps tendon were preserved. Stainless steel intramedullary rods were fixed, using polymethylmethacrylate bone cement (Simplex rapid, Austenal Dental Products, Harrow, UK), into the femurs and tibias.

TABLE 1

TABLE 1

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Patellar Tendon Elongation Measurement

The proximal end of the femoral rod was fixed in a steel frame in a materials test machine (model 1122, Instron, High Wycombe, UK). The knees were mounted with the femur upright. The tibia could flex freely in the sagittal plane and secondary degrees of freedom were unrestrained. The quadriceps tendon was connected to the load cell of the test machine via a liquid CO2 freezing clamp 15 and universal joint. Access to the posterior aspect of the patella and patellar tendon was gained through a lateral parapatellar incision in the retinaculum which did not cause any noticeable alteration of the patellofemoral tracking during loading of the extensor mechanism.

To measure patellar tendon elongation, the straight needle of a 2/0 polypropylene suture (Prolene, Ethicon, Somerville, NJ) was inserted in the patellar bone, at the point of attachment of the most posterior midline fibers of the patellar tendon (Fig 1). The needle was embedded fully in bone. Another suture was fixed in the same way at the patellar attachment of the midline fiber in the anterior layers (Fig 2A). This was not in the most superficial layer, because this continued proximally into the quadriceps without attaching to the patella, 2 but in the immediately underlying layer. Both sutures followed the course of the corresponding fiber bundles distally. The posterior suture was routed anteriorly through the distal end of the tendon, close to the bone (Fig 2B) and could slide freely through the tendon during testing. The sutures transmitted the length changes occurring in the anterior and posterior regions of the patellar tendon to a linear displacement transducer during quadriceps loading. An adjustable mounting on the tibial intramedullary rod allowed the displacement transducer to be aligned with each of the sutures. One suture at a time was attached to the displacement transducer. Each suture was kept at approximately 1 N tension tare load by connecting a rubber band to the moving core of the transducer. Thus, the suture did not change length, but transmitted changes in the distance between the bone attachments. The fiber strain was calculated by dividing the change in length of the fiber, measured by the linear transducer, divided by the unloaded fiber length, with a tare load applied.

Fig 1.

Fig 1.

Fig 2A–B.

Fig 2A–B.

To control the knee extension during quadriceps loading, a crossbar was placed through a slot in the vertical metal plate of the knee-mounting fixture at a radius of 140 mm from the femoral epicondyle, and the tibial intramedullary rod pressed against it. (Fig 3). This arrangement allowed the distal end of the suture and the transducer core to move in response to any change in the distance between the patellar tendon fiber attachments. The suture was subject only to the constant tare load, and so its elongation was not affected by the experiments.

Fig 3.

Fig 3.

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Extensor Mechanism Loading Experiment

The quadriceps was loaded cyclically 30 times from 50 N to 1 kN tension at a speed of 1000 mm/minute. The patellar tendon fiber length changes were monitored by the displacement transducer. The fiber length then was measured with a tare load of 50 N tension applied to the quadriceps. Measurements were taken as an average of four bone-to-bone measurements, using a caliper, from the point of insertion of the suture needle to the tibial attachment of the corresponding fiber. The voltage output from the displacement transducer was converted into millimeters of displacement by calibration with the moving core of the transducer resting on the endface of a micrometer spindle, giving length change accuracy better than +/− 0.1 mm. The joints were tested at 10°, 60°, and 90° flexion. Flexion angle was measured with a mechanical goniometer with an accuracy of +/− 1°, using the femoral and tibial rods as a reference. During loading and unloading, approximately 10° extension and flexion motion occurred in the knees, because of realignment of the tibia under load. Data were collected on a personal computer with a National Instruments LabData acquisition card (National Instruments, Berkshire, UK), using National Instruments LabWindows software.

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Determination of Material Properties

After the first study, 10 mm wide midline patella-patellar tendon-tibia blocks were isolated from the same knees. The patellar tendons were divided in the coronal plane into two parts with approximately equal thickness, and the patellar blocks were cut in line with the split between the fibers (Fig 4). The tibial end of the specimen was kept attached to the tibial block (Fig 4). The patellar and tibial blocks were potted in aluminum tubes and oriented so that the tendon pulled in a physiologic direction. Acrylic cement was poured into the tubes, so that it covered the bone entirely.

Fig 4.

Fig 4.

The cross-sectional area of the patellar tendon specimens was measured using a molding technique. 14 Each tendon unit was hung from the patellar block, with the potted tibial block pulling the fibers taut. Cement replicas of the bundles were made by: (1) pouring silicone rubber (Silcoset 105 with rapid curing agent, Ambersil, Bridgewater, UK) into a cardboard tube around the specimen; (2) removing the rubber mold from the tendon by splitting it longitudinally; and (3) by pouring liquid bone cement into the silicone mold. The cement replica was removed from the silicone mold and sawed transversely at its middle region. The section was photographed with a steel ruler in the same plane. The section was traced onto graph paper, along with a 10 mm reference, magnified 10 times. The cross-section was determined by counting the squares enclosed. 14

The patellar tendon fibers of the first two specimens tested avulsed from bone without failing. This was thought to reflect the ages of the specimens and associated bone loss. After this, the strips of tendon were cut from the remaining bone blocks and gripped at both ends with freezing jaws 15 in the materials test machine. The specimen was conditioned by loading and unloading 30 times, with a crosshead speed of 100 mm/minute, between 1 N and 100 N. The gauge length between the clamps was measured at 1 N tension after conditioning. The specimen then was loaded to failure at a speed of 1000 mm/minute. Tissue elongation during testing was measured as clamp-to-clamp displacement. The load versus crosshead displacement data were entered in a computer.

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Statistical Analysis

The differences in lengths of anterior and posterior fibers were compared using Student’s paired t test, and elongation and strain were compared using analysis of variance. The Wilcoxon signed rank sum test (matched pairs) was used to test the difference in structural and material properties. Significance was p < 0.05.

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RESULTS

Tendon Strain

The anterior fibers of the patellar tendon were significantly longer than the posterior fibers (p < 0.0001). The elongation and strain at 1 kN quadriceps load are shown in Table 2. There was no significant difference between elongations of anterior and posterior fibers at each angle of knee flexion (p > 0.2). However, as knee flexion increased, the difference in strain between the anterior and posterior fibers became progressively more significant (p = 0.61 at 10° knee flexion; p = 0.04 at 60°; p = 0.003 at 90°).

TABLE 2

TABLE 2

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Tensile Tests

All bundles ruptured by fiber failure between the clamps. There was no significant difference between the structural properties of the anterior and posterior specimens (p > 0.05;Table 3), although the posterior bundles tended to extend more before failure, despite being shorter. Among the material properties, the posterior fibers reached a significantly higher strain before failure than the anterior fibers (p = 0.002;Table 3) and tended to have a higher linear strain (p = 0.08), but otherwise there was no significant difference (p > 0.09).

TABLE 3

TABLE 3

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DISCUSSION

The pathogenesis of patellar tendonitis is debatable. 5 The lesions tend to affect the posterior, central, proximal part of the patellar tendon. 3,9,11 The central posterior fibers of the patellar tendon are the shortest, because of the shapes and orientations of the bone attachments. 2 Because patellar tendon elongation is likely to affect all fibers similarly, it follows that this will lead to the shortest fibers being subjected to the highest tensile strains in use, because strain is the elongation divided by the original fiber length. The hypothesis that patellar tendonitis may be related to tensile strain fits well with the common observation that the clinical problem results from repetitive tension overload.

The experiments in the current study found a significant difference in strain between the anterior and posterior fibers at the midline of the patellar tendon, when the knee extensor mechanism was loaded at greater angles of knee flexion, as was hypothesized. The significant findings were at 60° and 90° knee flexion, which encompass the range observed when landing from a jump. 10 However, although the posterior fibers of the patellar tendon had been subjected to significantly higher strains, the tensile tests then showed that they could withstand a significantly greater strain before they ruptured, and this was contrary to the second hypothesis. Thus, it appears that the posterior fibers are functionally adapted to withstand the greater strains found there. Taken together, the findings cast doubt on tensile strain alone being a significant pathogenetic factor in patellar tendonitis. The effects of larger strain cycles on tissue homeostasis are not known, and it may be speculated that large strain cycles may be related to a deleterious biologic reaction, but that is beyond the scope of this paper.

Experiments in vitro must try to reproduce real situations as closely as possible, and the current study had some limitations. One limitation is that the specimens were older than the relevant clinical population, and this may have caused the avulsion failures seen. Noyes et al 12 tested patellar tendon specimens from subjects aged 26 +/− 6 years and reported a higher failure stress, but that difference may result partly from the method used to measure specimen cross-sectional area. 14 Johnson et al 8 found that age had no significant effect on the tensile properties of the patellar tendon, apart from a 17% loss of failure strength between groups of subjects aged 29 to 50 years and 64 to 93 years. The failure strains in the current study were within the range of previous reports. 12,16 A prior study by the current authors (not published) found that some specimens were damaged above 1 kN quadriceps tendon load, and so the load applied was limited to 1 kN. The damage was attributable to avulsion from the patella, and it is accepted that bone strength reduces significantly with increasing age. The progressive loss of bone strength with age suggests that the patellar avulsions seen were probably not related to patellar tendonitis in a young athletic population. Huberti et al 7 estimated a maximum isometric quadriceps tension of 3.2 kN, giving 2.8 kN in the patellar tendon at 60° knee flexion. If the current strain results are scaled to these loads, it suggests anterior and posterior fiber strains of 8.6% and 14.7%. Butler et al 4 found failure strains of 12% to 14%, although they did not report a specific depth through the thickness of the patellar tendon. This is similar to the current result for anterior fibers: 15% +/− 4%. Because a 22% strain to failure occurred posteriorly, this suggests that none of the fibers, anterior or posterior, approach failure under normal muscle loads. However, little is known about joint loading in sports activities, and Stacoff et al 17 found peak foot-ground forces of 6.5 kN when landing. This suggests that greater loads may act around the knee in sports that include jumping and landing, when eccentric muscle loading occurs. Another limitation of the current study was that the test machine had a maximum speed of 1000 mm/minute, and this gave lower knee extension rates than the peaks seen in jumping, that range from 300°–600°/second. 10 However, it is unlikely that strain rate effects, that apply similarly to the anterior and posterior fibers, will affect the significant strain differences found in the current study. Patellar tendon strain has been reported from imaging in vivo, 16 but the study found 6.6% strain at only approximately 0.2 kN tension. Because this already is above the 5% level reported to cause permanent elongation, 1 it is difficult to reconcile this result with the loads and forces noted above.

The methods used in experiments are subject to errors apart from the differences that arise because of test conditions differing from reality in vivo. The principal sources of error in the current study concern the estimation of tensile properties. The load signal was accurate to +/− 0.5%, and the specimen cross section was accurate to +/− 1.8%, 14 suggesting an error of +/− 2.3% in estimating failure stress. The specimen fibers were clamped directly because they avulsed from bone at submaximal loads. This led to errors at the specimen-clamp interface and to errors attributable to grip to grip compliance of the testing frame, estimated to be 4% or less. The freezing jaws were known to keep specimen slippage below the 0.1 mm resolution of the system in cyclic 6 and ultimate 13 tensile tests on tendons. Optical or miniature pinned-on extensometers were not used because observation showed erratic differences in strain behavior between fibers across the width of the specimen, so grip to grip displacement would be more representative of overall structural behavior. Noyes et al 12 found grip to grip strains larger than optical measurements of surface markers, in the midlength of their specimens, but their measurements may have included slippage of specimens from the grip. 12

Much higher strains have been reported near bone attachments, 12 but the link to patellar tendonitis still may be questioned, because this effect occurred at both ends of the patellar tendons and in other tendons. The bone avulsions associated with the specimens from elderly subjects that were available for this study prevented acquisition of patellar tendon failure strain data from the most proximal part of the tendon, that would relate best to tendonitis.

The current findings show that the posterior fibers of the patellar tendon are subjected to the greatest tensile strains when the quadriceps tendon is loaded with the knee flexed. However, they are not sufficient to explain why the lesions of patellar tendonitis usually are found proximally in these fibers. 5,9,11 It seems likely, therefore, that some other factors have a role. Noyes et al 12 found greater patellar tendon surface strains on the exterior aspect near the bone attachments, but these zones were clamped in the current tests, and it is not known if the same behavior occurs on the posterior aspect. Localized strain measurement in younger specimens would be appropriate. Another mechanical factor could be transverse pressure imposed by the distal tip of the patella against the posterior aspect of the patellar tendon as the knee flexes. 9 Biologic factors, such as regional variation in vascularity, may be relevant. Additional study is needed to better understand how soft tissues adapt to strain cycles in use, and the pathogenesis of the classic lesions of patellar tendonitis.

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Acknowledgments

The materials test machine was donated by the Arthritis Research Campaign, a charity based at Chesterfield, England.

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