Cell Tissue Bank DOI 10.1007/s10561-014-9421-5
ORIGINAL PAPER
Quadriceps tendon allografts as an alternative to Achilles tendon allografts: a biomechanical comparison Isaac Mabe • Shawn Hunter
Received: 30 September 2013 / Accepted: 3 January 2014 Ó Springer Science+Business Media Dordrecht 2014
Abstract Quadriceps tendon with a patellar bone block may be a viable alternative to Achilles tendon for anterior cruciate ligament reconstruction (ACL-R) if it is, at a minimum, a biomechanically equivalent graft. The objective of this study was to directly compare the biomechanical properties of quadriceps tendon and Achilles tendon allografts. Quadriceps and Achilles tendon pairs from nine research-consented donors were tested. All specimens were processed to reduce bioburden and terminally sterilized by gamma irradiation. Specimens were subjected to a three phase uniaxial tension test performed in a custom environmental chamber to maintain the specimens at a physiologic temperature (37 ± 2 °C) and misted with a 0.9 % NaCl solution. There were no statistical differences in seven of eight structural and mechanical between the two tendon types. Quadriceps tendons exhibited a significantly higher displacement at maximum load and significantly lower stiffness than Achilles tendons. The results of this study indicated a biomechanical equivalence of aseptically processed, terminally sterilized quadriceps tendon grafts with bone block to Achilles tendon grafts with bone block. The significantly higher displacement at maximum load, and lower stiffness observed for quadriceps tendons may be related to the failure mode. Achilles I. Mabe (&) S. Hunter Community Tissue Services, 2900 College Dr., Kettering, OH 45420, USA e-mail: [email protected]
tendons had a higher bone avulsion rate than quadriceps tendons (86 % compared to 12 %, respectively). This was likely due to observed differences in bone block density between the two tendon types. This research supports the use of quadriceps tendon allografts in lieu of Achilles tendon allografts for ACL-R. Keywords Allograft Anterior cruciate ligament reconstruction Quadriceps tendon Achilles tendon Biomechanics
Introduction Anterior cruciate ligament (ACL) tears occur at an estimated rate of one in 3,000 annually in the United States (Freedman et al. 2003). Damage to the ligament alters the natural biomechanical behavior of the knee, increasing the incidence of meniscal damage and the risk of developing osteoarthritis (Tashman et al. 2008). Surgical intervention is often required resulting in the need for more than 100,000 anterior cruciate ligament reconstructions (ACL-R) every year. As a result of the large numbers of tears, ACL-R is a common procedure with a history of positive clinical outcomes (Liu et al. 1995; Santori et al. 2004). Both autografts and allografts are used in ACL-R, and their advantages and disadvantages have been both identified and debated (Belisle et al. 2007; Freedman et al. 2003; Hamner et al. 1999; Nicklin
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et al. 2000; Scheffler et al. 2002; Shelton and Fagan, 2001; West and Harner 2005). Common autografts of bone-patellar tendon-bone (BPTB) and semitendinosus tendons (Siebold et al. 2003) have the advantage of host incorporation and biologic vascularization. However, autografts suffer from donor site morbidity, and in cases of BPTB autograft use there are reports of quadriceps weakness, anterior knee pain and patellar fractures (Liu et al. 1995; Santori et al. 2004). Allografts including quadriceps tendons, semitendinosus, gracilis, anterior/posterior tibialis, Achilles tendons, and BPTBs represent other options for ACL-R (Dargel et al. 2006; Han et al. 2008b; Schatzmann et al. 1998), with the latter two tendons being the more popular allografts currently used (Siebold et al. 2003). While allografts tend to require longer times for biologic vascularization and integration (West and Harner 2005), they do have advantages of a wider variety of sizes and avoid donor site morbidity that can lead to infections or the need to rehabilitate the autograft harvest site (Santori et al. 2004; Schindler 2012; West and Harner 2005). Quadriceps tendon grafts, first described by Marshall (Marshall et al. 1979), have been used in ACL-R since the 1980s when they were popularized by Blauth (Staubli et al. 1999). Similar to the Achilles tendon, quadriceps tendons can be recovered with a bony attachment and have large widths and lengths that make them an attractive graft option. The quadriceps tendon’s substantial cross sectional area prevents synovial bathing, which has been shown to stimulate osteoclast activity causing bone resorption through the inflow of cytokines (Paessler and Mastrokalos 2003). The inclusion of the patellar bone block becomes advantageous for surgeons looking for a point of strong fixation (Scheffler et al. 2002). Biomechanically the quadriceps tendon exhibits similar properties as the BPTB in stiffness and ultimate load to failure (Dargel et al. 2006; Staubli et al. 1996; West and Harner 2005). Quadriceps grafts are comparable to BPTBs in flexion deficits, activity reduction, and side-to-side torque ratios postoperatively (Han et al. 2008b), and overall they have exhibited positive clinical results (Howe et al. 1991; Kaplan et al. 1991). Recent studies have shown that quadriceps autografts yield similar clinical outcomes and biomechanical properties to more commonly used BPTB autografts (Geib et al. 2009) and Achilles tendons (Lewis and Shaw 1997; Siebold et al. 2003).
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However, a corresponding increase in quadriceps allograft usage has yet to be noticed. This may in part be due to insufficient quadriceps allograft characterization since most studies have examined the anatomy and mechanical properties of fresh cadaveric tendons (Dargel et al. 2006; Harris et al. 1997; Staubli et al. 1996) and not those that have undergone aseptic processing and sterilization treatments commonly employed by tissue banks. Therefore, the purpose of this study was to determine the biomechanical properties of quadriceps tendon allografts and compare them to those of Achilles tendon allografts. Our hypothesis was that quadriceps tendon allografts would not be biomechanically different from Achilles tendon allografts. Results that support our hypothesis would indicate that quadriceps tendon allografts may be suitable for use in ACL-R.
Materials and methods Specimen preparation One Achilles tendon with bone blocks and one quadriceps tendon with bone blocks was procured per donor from a total of nine research-consented donors (nine males, mean age 56.1 years, range 37–74 years) and aseptically processed as freshfrozen grafts per current soft tissue standard manufacturing procedures. These procedures included a proprietary bio-burden reduction treatment (AllowashÒ; LifeNet Health. Virginia Beach, VA). All specimens were terminally sterilized via gamma irradiation using a 9.2–11.0 kGy dose range. This sterilization method has been validated following ISO Standard 11137-2 Method 2B (ISO 11137-2:2006,) to achieve a sterility assurance level (SAL) of 10-6. Tendons were stored at B-65 °C until biomechanical testing. Specimens were thawed in a 37 °C water bath for no more than 15 min prior to testing. For both tendon types, the central 10 mm of the bone-tendon complex was isolated using a band saw and scalpel (Dargel et al. 2006; Schatzmann et al. 1998; Staubli et al. 1996, 1999). Quadriceps tendons were further trimmed by sharp dissection to isolate the tightly connected bundles of the rectus femoris and the vastus intermedius in accordance with clinical preparations (Geib et al. 2009). The resulting shape of the tendons was rectangular in cross section. The bone blocks of all
Cell Tissue Bank
Misting Nozzle
Specimen
Pneumatic Grips
Fig. 1 Custom environmental testing chamber with recirculating fluid spray and temperature control
specimens were then potted using a body filler resin (BondoÒ; 3M; St. Paul, MN) in custom molds to increase the grip surface in order to prevent slippage during testing. The opposite free end of the tendon was wrapped in a strip of 220 grit sandpaper augmented with cyanoacrylate to affix the sandpaper to the tendon. This was done to increase the friction between the tendon and the pneumatic gripping faces in an effort to prevent tendon slippage. Biomechanical testing At testing, tendon cross sectional area was measured using digital micrometers in an unloaded state. Three measurements were taken of the width and base along the length at three discrete points and averaged. The specimen was then placed in an environmental testing chamber (Fig. 1) that maintained a physiologic environment at 37 ± 2 °C and misted the specimen with 0.9 % sodium chloride solution for the testing duration. Once the specimen was secured in the pneumatic grips, an initial gage length was measured between the inside edges of each grip using a steel ruler. The steel ruler had an accuracy of 1/64 in. (0.4 mm). All specimens were placed in the Instron with approximately 50 mm (1.97 in.) of gage length. This gives a possible error of 0.8 % if the ruler accuracy is considered at 1.97 in.. The shortest gauge length was 1.75 in., for which the largest measuring error of 0.9 % was deemed acceptable for the nature of the testing. Each specimen was placed in the grips such that a consistent length-to-width ratio of approximately 5:1 was maintained. Biomechanical testing was performed using a materials testing system (ElectroPuls E3000; Instron, Norwood, MA). To mimic different physiologic
loading scenarios, the testing system was programmed with a three-phase uniaxial tension loading protocol using Bluehill Wavematrix software (v. 1.4; Instron, Norwood, MA). The first phase was a sinusoidal wave that was load-controlled between 0 and 200 N at a 2 Hz frequency for 2,000 cycles, and was designed to replicate a cyclic sub-failure load on the ACL analogous to a moderate activity (i.e. a brisk walk). The second phase was a 5 min stationary rest period to allow for tendon recovery. The last phase was a linear ramp to failure at a displacement-controlled rate of 100 % strain per second to simulate a catastrophic injury (Hoburg et al. 2010). The method of failure was recorded. Biomechanical property calculations Structural and material properties were calculated from load–displacement and stress–strain curves, respectively, for each specimen. Maximum load and displacement at the maximum load were recorded for each specimen. Stiffness was calculated as the linear portion of the load–displacement curve in the failure phase of testing. The calculation was consistently performed for all the specimens. Stress was calculated as the force applied to the tendon divided by the measured cross sectional area. The maximum stress and the corresponding strain at maximum stress were reported. Strain was calculated by measuring the initial grip to grip distance between the faces of the pneumatic grips. The tendon lengthened after the cyclic phase of the test and not all of this additional length was recovered in the relaxation phase of the test; however the tendon was not physically remeasured. To account for the additional length from the cyclic phase in the ramp-to-failure phase, the displacement at a 1 N tare load was added to the original measured gage length. To calculate the strain in the ramp-to-failure phase, displacement was divided by the summation of the initial gage length plus the additional accrued length from the cyclic phase (DL/(Linitial ? Ladditional)). Similar to stiffness, the modulus of elasticity was calculated as the linear portion of the stress–strain curve in the failure phase. The percent difference in elongation of the tissue after the cyclic phase of the test was calculated as ((L2000 - L10)/L10) 9 100. The 10th cycle peak was picked to account for initial preconditioning of the tendon. The 2,000th cycle was chosen unless the
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tendon failed in the sub-failure phase. If the specimen failed before the ramp-to-failure phase, the second to last peak was used for calculations as the last cycle would be the load to failure ramp.
(p = 0.139) and cyclic elongation (p = 0.054) exhibited no significant differences between tendon types.
Discussion Statistical analysis Mean and standard deviation were calculated for the maximum load, displacement at maximum load, stiffness, maximum stress, strain at maximum stress, modulus, and cyclic elongation data for each tendon type. A paired t test was conducted to analyze the potential differences between the groups using statistical software (SigmaPlot 12.3; Systat Software, San Jose CA). A difference was considered significant if the calculated p-value was less than a two-tailed a of 0.05.
Results Two Achilles grafts and one quadriceps graft failed during the cyclic testing phase by bone avulsion and were subsequently excluded from analysis. The Achilles specimens failed at cycle number 570 and 993 while the quadriceps specimen failed at cycle number 1,050. All remaining specimens failed during the final ramp-to-failure phase. All specimens failed either by bone avulsion or by a tendon mid-substance rupture, and no slippage or soft tissue failure at the grips was observed during the testing duration. Six of seven Achilles allografts (86 %) failed by bone avulsion and the remaining specimen failed due to mid-substance tendon rupture. Conversely, seven of eight quadriceps allografts (88 %) failed by tendon mid-substance rupture with the other two specimens failing by bone avulsion. Structural properties for the quadriceps and Achilles tendons are summarized in Table 1. No significant differences were detected between tendon types for cross-sectional area (p = 0.721) and maximum load (p = 0.413). Quadriceps grafts had a significantly higher displacement at maximum load (p = 0.040) than Achilles grafts with a 1.09 mm difference between mean values. Quadriceps also had a significantly lower and stiffness (p = 0.029) than Achilles with a difference of 56.16 N/mm. Similarly, material properties for the quadriceps and Achilles tendons are summarized in Table 2. Maximum stress (p = 0.366), strain at maximum stress (p = 0.072), modulus
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Having multiple graft options is advantageous for meeting the steadily increasing demand of ACL-R procedures. Allografts offer an abundant volume of tissue without the complications of donor site morbidity, and advances in donor screening, aseptic processing and terminal sterilization have decreased the risk of disease transmission. Both Achilles and quadriceps tendon allografts offer ample soft tissue with a bone plug for secure fixation, but quadriceps tendon graft use has surprisingly trailed that of Achilles tendon grafts. This direct, biomechanical comparison of quadriceps and Achilles tendon allografts showed no statistically significant differences in six out of eight structural and material properties in an effort to promote quadriceps tendon as a practical graft alternative. Material and structural properties of non-irradiated, fresh frozen quadriceps and Achilles tendons have been reported (Dargel et al. 2006; Harris et al. 1997; Lewis and Shaw 1997; Staubli et al. 1996; Wren et al. 2001). Maximum load to failure is one property of clinical relevance since it represents the tissue’s capacity for resisting and transmitting loads. For quadriceps tendon, our maximum load to failure results (830.14–1797.02 N) were consistent with the range of 131–2353 N (Staubli et al. 1996) cited in the literature. Additionally, our quadriceps tendon allografts exhibited displacements at maximum load of 8.36 ± 0.81 mm and strains at maximum stress of 16 ± 2 % that were comparable to displacements [5.9 ± 1.2 mm (Schatzmann et al. 1998)] and strains [14.7 ± 3.7 % (Staubli et al. 1999)] reported in the literature. For Achilles tendons, our maximum load results (397.49–1349.92 N) overlapped the lower end of the reported range of 843–5194 N (Lewis and Shaw 1997; Wren et al. 2001) and our displacement at maximum load (5.06–15.43 mm) included, but was broader than, the reported range of 1.8–8.7 mm (Lewis and Shaw 1997). Both the quadriceps and the Achilles tendon strain at maximum stress (15.0 ± 7 and 16 ± 2 %, respectively) are consistent with reported ACL strains at maximum stress of 15–19 % (Butler et al. 1986).
Cell Tissue Bank Table 1 Structural properties (mean ± SD) Cross-sectional area (mm2)
Max load (N)
Disp. @ max load (mm)
Stiffness (N/mm)
Achilles tendon
55.2 ± 5.8
915 ± 326
7.57 ± 3.62
217 ± 45
Quadriceps tendon
57.4 ± 14.7
1055 ± 313
8.36 ± 0.81
161 ± 48
p value Significance
0.721 NS
0.413 NS
0.040 Significant
0.029 Significant
Table 2 Material Properties (mean ± SD)
Achilles tendon
Max stress (MPa)
Strain @ max stress (mm/mm)
Modulus (MPa)
Cyclic elongation (%)
16.0 ± 7.32
0.15 ± 0.07
201 ± 70
1.29 ± 0.50 1.97 ± 0.69
Quadriceps tendon
19.1 ± 5.42
0.16 ± 0.02
153 ± 46
p value
0.366
0.072
0.139
0.054
Significance
NS
NS
NS
NS
These differences were likely due to variations in the boundary conditions of our test methodology compared to those in the literature. In an effort to replicate clinically relevant failures, the bone blocks of specimens in this study were potted without constraining the bone-tendon interface to allow for failures such as bone avulsions to occur. Other studies often embedded the bone blocks in castings or metal fixtures to restrain the bone block (Lewis and Shaw 1997; Staubli et al. 1999; Wren et al. 2003), which likely drove failure loads (and corresponding failure stresses) higher by artificially forcing failure paths from the bone-tendon interface to the stronger tendon. Our investigation of cyclic elongation is clinically valuable because it characterized the amount of slack a tendon graft accrues after repeated subfailure loading analogous to some activities of daily living. Quadriceps and Achilles tendons in this study demonstrated similar elongations of 1.97 and 1.29 %, respectively, which corresponded to mean changes of 0.99 and 0.64 mm. Such minimal changes in graft length are important for maintaining the relative anatomic positions of the femur and tibia during postsurgical activities. It is noted that three specimens failed by bone avulsion during the cyclic loading phase and therefore were excluded from the analysis. This exclusion was justified since the resulting elongation could not be attributed solely to the tendon but rather included separation of the bone block and tendon realignment as it rotated to resist the applied tensile force, and failing by
a different strain rate than the load to failure protocol. These premature failures may have been a byproduct of our gripping configuration, which as previously stated made the specimens susceptible to failure by bone avulsion. Displacement at maximum load and stiffness were the only significantly different biomechanical properties observed in this study. The differences may be attributable to contrasts in how each tendon type is attached to their respective bone blocks. The quadriceps tendon attaches to the dense cortical bone of the patella while the Achilles tendon attaches to more porous cancellous bone of the calcaneus. Our observation that quadriceps grafts had only a 12.5 % bone avulsion rate compared to an 86 % avulsion rate for Achilles tendons suggests that the latter abruptly fails at the bone block before it has the ability to reach the same maximum load and having a similar displacement at the maximum load. The larger displacement and lower stiffness observed for quadriceps tendons may indicate that the patella-tendon interface is stronger than that of the Achilles, which thereby shifts the failure initiation to the tendon as supported by the higher occurrences of mid-substance rupture. One limitation of this study was that all specimens were procured from male donors, so any potential gender-based differences could not be examined. This was not intentional as specimens were randomly selected from a pool of research-consented donors, but instead is representative of our tissue bank’s donor population that is historically two-thirds male. We do
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not feel that this is an issue as other studies performed in our laboratory have not shown biomechanical differences in BTB and tibialis allografts due to donor gender (data submitted for publication). Additionally this study is statistically underpowered. Initial study design considered outcomes of previous research and the sample sizes were designed to achieve a power of 0.80. Due to sample size reduction from cyclic load failures and variation in the results a post hoc power analysis indicated an underpowered test. Lack of power is a recognized limitation of this study. This study also only addresses the grafts’ time zero biomechanical properties, which cannot be extrapolated to longer term, clinical graft performance influenced by biologic healing responses. Our testing was conducted on an isolated tendon section rather than the entire tendon. Initial attempts to test whole grafts were unsuccessful due to limitations in our gripping system, and after observing a high incidence of failures caused by the grips we revised our specimen design. The quadriceps tendons proved especially challenging since they are comprised of multiple connected bundles. Our isolation of the central third of the rectus femoris and the vastus intermedius bundles emulated reported clinical procedures for graft preparation (Han et al. 2008a; Santori et al. 2004; West and Harner 2005), and the corresponding Achilles grafts were fashioned in the same manner to produce similar specimens for comparison. Should clinicians choose to utilize all bundles of the quadriceps tendon the increased tissue mass could bolster the graft’s biomechanical capabilities. In conclusion, based on the observed equivalence of biomechanical results and anatomical similarities, our recommendation is that quadriceps tendon allografts are biomechanically equivalent to Achilles tendon allografts when they are both aseptically processed and terminally sterilized with gamma irradiation. A history of positive clinical outcomes for quadriceps tendon autografts in ACL-R also suggests that quadriceps tendon allografts may yield favorable clinical results.
References Belisle A, Bicos J, Geaney L, Anderson M, Obopilwe E, Rincon L et al (2007) Strain pattern comparison of double- and
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singlebundle anterior cruciate ligament reconstruction techniques with the native anterior cruciate ligament. Arthroscopy 23(11):1210–1217 Butler DL, Kay MD, Stouffer DC (1986) Comparison of material properties in fascicle-bone units from human patellar tendon and knee ligaments. J Biomech 19(6):425–432 Dargel J, Schmidt-Wiethoff R, Schneider T, Bruggemann G, Koebke J (2006) Biomechanical testing of quadriceps tendon-patellar bone grafts: an alternative graft source for press-fit anterior cruciate ligament reconstruction? Arch Orthop Trauma Surg 126:265–270 Freedman K, D’Amato M, Nedeff D, Kaz A, Bach B (2003) Arthroscopic anterior cruciate ligament reconstruction: a metaanalysis comparing patellar tendon and hamstring tendon autografts. Am J Sports Med 31(1):2–11 Geib T, Shelton W, Phelps R, Clark L (2009) Anterior cruciate ligament reconstruction using quadriceps tendon autograft: intermediate-term outcome. Arthroscopy 25(12):1408– 1414 Hamner D, Brown C, Steiner M, Hecker A, Hayes W (1999) Hamstring tendon grafts for reconstruction of the anterior cruciate ligament: Biomechanical evaluation of the use of multiple strands and tensioning techniques. J Bone Joint Surg Am 81(A(4)):549–557 Han HS, Seong SC, Lee S, Lee MC (2008a) Anterior cruciate ligament reconstruction. Clin Orthop Relat Res 466:198– 204 Han HS, Seong SC, Lee S, Lee MC (2008b) Anterior cruciate ligament reconstruction : quadriceps versus patellar autograft. Clin Orthop Relat Res 466(1):198–204 Harris L, Smith D, Lamoreaux L, Purnell M (1997) Central quadriceps tendon for anterior cruciate reconstruction. Am J Sports Med 25(1):23–28 Hoburg AT, Keshlaf S, Schmidt T, Smith M, Gohs U, Perka C et al (2010) Effect of electron beam irradiation on biomechanical properties of patellar tendon allografts in anterior cruciate ligament reconstruction. Am J Sports Med 38(6):1134–1140 Howe J, Johnson R, Kaplan M (1991) Anterior cruciate ligament reconstruction using quadriceps patellar tendon graft. Part I: long-term follow up. Am J Sports Med 7:801–811 ISO 11137-2:2006 Sterilization of health care products-radiation-Part 2: establishing the sterilization dose Kaplan M, Howe J, Flemming B, Johnson R, Jarinen M (1991) Anterior cruciate ligament reconstruction using quadriceps patellar tendon graft. Part II: a specific sport review. Am J Sports Med 19(5):458–462 Lewis G, Shaw K (1997) Tensile properties of human tendo Achillis: effect of donor age and strain rate. J Foot Ankle Surg 36(6):435–445 Liu S, Kabo M, Osti L (1995) Biomechanics of two types of Bone-tendon-bone graft for ACL reconstruction. J Bone Joint Surg (Br) 77-B:232–235 Marshall J, Warren R, Wickiewicz T, Reider B (1979) The anterior cruciate ligament: a technique of repair and reconstruction. Clin Orthop 19:458–462 Nicklin S, Waller C, Walker P, Chung W, Walsh W (2000) In vitro structural properties of braided tendon grafts. Am J Sports Med 28(6):790–793 Paessler H, Mastrokalos D (2003) Anterior cruciate ligament reconstruction using semitendinosus and gracilis tendons,
Cell Tissue Bank bone patellar tendon, or quadriceps tendon-graft with press fit fixation without hardware, a new and innovative procedure. Orthop Clin N Am 34:49–64 Santori N, Adriani E, Pederzini L (2004) ACL reconstruction using quadriceps tendon. Orthopedics 27(1):31–35 Schatzmann L, Brunner P, Staubli HU (1998) Effect of cyclic preconditioning on the tensile properties of human quadriceps tendons and patellar ligaments. Knee Surg Sports Traumatol Arthrosc 6(Suppl 1):S56–S61 Scheffler S, Sudkamp N, Gockenjan A, Hoffmann R, Weiler A (2002) Biomechanical comparison of hamstring and patellar tendon graft anterior cruciate ligament reconstruction techniques: the impact of fixation level and fixation method under cyclic loading. Arthroscopy 18(3): 304–315 Schindler A (2012) Surgery for anterior cruciate ligament deficiency: a historical perspective. Knee Surg Sports Traumatol Arthrosc 20:5–47 Shelton W, Fagan B (2001) Autografts commonly used in anterior cruciate ligament reconstruction. J Am Acad Orthop Surg 19(5):259–264 Siebold R, Buelow JU, Bos L, Ellerman A (2003) Primary ACL reconstruction with fresh-frozen patellar versus Achilles tendon allografts. Arch Orthop Trauma Surg 123:180–185
Staubli H, Schatzmann L, Brunner P, Rincon L, Nolte L (1996) Quadriceps tendon and patellar ligament: cryosectional anatomy and structural properties in young adults. Knee Surg Sports Traumatol Arthrosc 4:100–110 Staubli H, Schatzmann L, Brunner P, Rincon L, Nolte L (1999) Mechanical tensile properties of the quadriceps tendon and patellar ligament in young adults. Am J Sports Med 27(1):27–34 Tashman S, Kopf S, Fu F (2008) The kinematic basis of anterior cruciate ligament reconstruction. Oper Tech Sports Med 16(3):116–118 West R, Harner C (2005) Graft Selection in anterior cruciate ligament reconstruction. J Am Acad Orthop Surg 13:197–207 Wren T, Yerby S, Beaupre G, Carter D (2001) Mechanical properties of the human aachilles tendon. Clin Biomech 16:245–251 Wren T, Lindsey D, Beaupre G, Carter D (2003) Effects of creep and cyclic loading on the mechanical properties and failure of human achilles tendon. Ann Biomed Eng 31:710–717
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ORIGINAL PAPER
Quadriceps tendon allografts as an alternative to Achilles tendon allografts: a biomechanical comparison Isaac Mabe • Shawn Hunter
Received: 30 September 2013 / Accepted: 3 January 2014 Ó Springer Science+Business Media Dordrecht 2014
Abstract Quadriceps tendon with a patellar bone block may be a viable alternative to Achilles tendon for anterior cruciate ligament reconstruction (ACL-R) if it is, at a minimum, a biomechanically equivalent graft. The objective of this study was to directly compare the biomechanical properties of quadriceps tendon and Achilles tendon allografts. Quadriceps and Achilles tendon pairs from nine research-consented donors were tested. All specimens were processed to reduce bioburden and terminally sterilized by gamma irradiation. Specimens were subjected to a three phase uniaxial tension test performed in a custom environmental chamber to maintain the specimens at a physiologic temperature (37 ± 2 °C) and misted with a 0.9 % NaCl solution. There were no statistical differences in seven of eight structural and mechanical between the two tendon types. Quadriceps tendons exhibited a significantly higher displacement at maximum load and significantly lower stiffness than Achilles tendons. The results of this study indicated a biomechanical equivalence of aseptically processed, terminally sterilized quadriceps tendon grafts with bone block to Achilles tendon grafts with bone block. The significantly higher displacement at maximum load, and lower stiffness observed for quadriceps tendons may be related to the failure mode. Achilles I. Mabe (&) S. Hunter Community Tissue Services, 2900 College Dr., Kettering, OH 45420, USA e-mail: [email protected]
tendons had a higher bone avulsion rate than quadriceps tendons (86 % compared to 12 %, respectively). This was likely due to observed differences in bone block density between the two tendon types. This research supports the use of quadriceps tendon allografts in lieu of Achilles tendon allografts for ACL-R. Keywords Allograft Anterior cruciate ligament reconstruction Quadriceps tendon Achilles tendon Biomechanics
Introduction Anterior cruciate ligament (ACL) tears occur at an estimated rate of one in 3,000 annually in the United States (Freedman et al. 2003). Damage to the ligament alters the natural biomechanical behavior of the knee, increasing the incidence of meniscal damage and the risk of developing osteoarthritis (Tashman et al. 2008). Surgical intervention is often required resulting in the need for more than 100,000 anterior cruciate ligament reconstructions (ACL-R) every year. As a result of the large numbers of tears, ACL-R is a common procedure with a history of positive clinical outcomes (Liu et al. 1995; Santori et al. 2004). Both autografts and allografts are used in ACL-R, and their advantages and disadvantages have been both identified and debated (Belisle et al. 2007; Freedman et al. 2003; Hamner et al. 1999; Nicklin
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et al. 2000; Scheffler et al. 2002; Shelton and Fagan, 2001; West and Harner 2005). Common autografts of bone-patellar tendon-bone (BPTB) and semitendinosus tendons (Siebold et al. 2003) have the advantage of host incorporation and biologic vascularization. However, autografts suffer from donor site morbidity, and in cases of BPTB autograft use there are reports of quadriceps weakness, anterior knee pain and patellar fractures (Liu et al. 1995; Santori et al. 2004). Allografts including quadriceps tendons, semitendinosus, gracilis, anterior/posterior tibialis, Achilles tendons, and BPTBs represent other options for ACL-R (Dargel et al. 2006; Han et al. 2008b; Schatzmann et al. 1998), with the latter two tendons being the more popular allografts currently used (Siebold et al. 2003). While allografts tend to require longer times for biologic vascularization and integration (West and Harner 2005), they do have advantages of a wider variety of sizes and avoid donor site morbidity that can lead to infections or the need to rehabilitate the autograft harvest site (Santori et al. 2004; Schindler 2012; West and Harner 2005). Quadriceps tendon grafts, first described by Marshall (Marshall et al. 1979), have been used in ACL-R since the 1980s when they were popularized by Blauth (Staubli et al. 1999). Similar to the Achilles tendon, quadriceps tendons can be recovered with a bony attachment and have large widths and lengths that make them an attractive graft option. The quadriceps tendon’s substantial cross sectional area prevents synovial bathing, which has been shown to stimulate osteoclast activity causing bone resorption through the inflow of cytokines (Paessler and Mastrokalos 2003). The inclusion of the patellar bone block becomes advantageous for surgeons looking for a point of strong fixation (Scheffler et al. 2002). Biomechanically the quadriceps tendon exhibits similar properties as the BPTB in stiffness and ultimate load to failure (Dargel et al. 2006; Staubli et al. 1996; West and Harner 2005). Quadriceps grafts are comparable to BPTBs in flexion deficits, activity reduction, and side-to-side torque ratios postoperatively (Han et al. 2008b), and overall they have exhibited positive clinical results (Howe et al. 1991; Kaplan et al. 1991). Recent studies have shown that quadriceps autografts yield similar clinical outcomes and biomechanical properties to more commonly used BPTB autografts (Geib et al. 2009) and Achilles tendons (Lewis and Shaw 1997; Siebold et al. 2003).
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However, a corresponding increase in quadriceps allograft usage has yet to be noticed. This may in part be due to insufficient quadriceps allograft characterization since most studies have examined the anatomy and mechanical properties of fresh cadaveric tendons (Dargel et al. 2006; Harris et al. 1997; Staubli et al. 1996) and not those that have undergone aseptic processing and sterilization treatments commonly employed by tissue banks. Therefore, the purpose of this study was to determine the biomechanical properties of quadriceps tendon allografts and compare them to those of Achilles tendon allografts. Our hypothesis was that quadriceps tendon allografts would not be biomechanically different from Achilles tendon allografts. Results that support our hypothesis would indicate that quadriceps tendon allografts may be suitable for use in ACL-R.
Materials and methods Specimen preparation One Achilles tendon with bone blocks and one quadriceps tendon with bone blocks was procured per donor from a total of nine research-consented donors (nine males, mean age 56.1 years, range 37–74 years) and aseptically processed as freshfrozen grafts per current soft tissue standard manufacturing procedures. These procedures included a proprietary bio-burden reduction treatment (AllowashÒ; LifeNet Health. Virginia Beach, VA). All specimens were terminally sterilized via gamma irradiation using a 9.2–11.0 kGy dose range. This sterilization method has been validated following ISO Standard 11137-2 Method 2B (ISO 11137-2:2006,) to achieve a sterility assurance level (SAL) of 10-6. Tendons were stored at B-65 °C until biomechanical testing. Specimens were thawed in a 37 °C water bath for no more than 15 min prior to testing. For both tendon types, the central 10 mm of the bone-tendon complex was isolated using a band saw and scalpel (Dargel et al. 2006; Schatzmann et al. 1998; Staubli et al. 1996, 1999). Quadriceps tendons were further trimmed by sharp dissection to isolate the tightly connected bundles of the rectus femoris and the vastus intermedius in accordance with clinical preparations (Geib et al. 2009). The resulting shape of the tendons was rectangular in cross section. The bone blocks of all
Cell Tissue Bank
Misting Nozzle
Specimen
Pneumatic Grips
Fig. 1 Custom environmental testing chamber with recirculating fluid spray and temperature control
specimens were then potted using a body filler resin (BondoÒ; 3M; St. Paul, MN) in custom molds to increase the grip surface in order to prevent slippage during testing. The opposite free end of the tendon was wrapped in a strip of 220 grit sandpaper augmented with cyanoacrylate to affix the sandpaper to the tendon. This was done to increase the friction between the tendon and the pneumatic gripping faces in an effort to prevent tendon slippage. Biomechanical testing At testing, tendon cross sectional area was measured using digital micrometers in an unloaded state. Three measurements were taken of the width and base along the length at three discrete points and averaged. The specimen was then placed in an environmental testing chamber (Fig. 1) that maintained a physiologic environment at 37 ± 2 °C and misted the specimen with 0.9 % sodium chloride solution for the testing duration. Once the specimen was secured in the pneumatic grips, an initial gage length was measured between the inside edges of each grip using a steel ruler. The steel ruler had an accuracy of 1/64 in. (0.4 mm). All specimens were placed in the Instron with approximately 50 mm (1.97 in.) of gage length. This gives a possible error of 0.8 % if the ruler accuracy is considered at 1.97 in.. The shortest gauge length was 1.75 in., for which the largest measuring error of 0.9 % was deemed acceptable for the nature of the testing. Each specimen was placed in the grips such that a consistent length-to-width ratio of approximately 5:1 was maintained. Biomechanical testing was performed using a materials testing system (ElectroPuls E3000; Instron, Norwood, MA). To mimic different physiologic
loading scenarios, the testing system was programmed with a three-phase uniaxial tension loading protocol using Bluehill Wavematrix software (v. 1.4; Instron, Norwood, MA). The first phase was a sinusoidal wave that was load-controlled between 0 and 200 N at a 2 Hz frequency for 2,000 cycles, and was designed to replicate a cyclic sub-failure load on the ACL analogous to a moderate activity (i.e. a brisk walk). The second phase was a 5 min stationary rest period to allow for tendon recovery. The last phase was a linear ramp to failure at a displacement-controlled rate of 100 % strain per second to simulate a catastrophic injury (Hoburg et al. 2010). The method of failure was recorded. Biomechanical property calculations Structural and material properties were calculated from load–displacement and stress–strain curves, respectively, for each specimen. Maximum load and displacement at the maximum load were recorded for each specimen. Stiffness was calculated as the linear portion of the load–displacement curve in the failure phase of testing. The calculation was consistently performed for all the specimens. Stress was calculated as the force applied to the tendon divided by the measured cross sectional area. The maximum stress and the corresponding strain at maximum stress were reported. Strain was calculated by measuring the initial grip to grip distance between the faces of the pneumatic grips. The tendon lengthened after the cyclic phase of the test and not all of this additional length was recovered in the relaxation phase of the test; however the tendon was not physically remeasured. To account for the additional length from the cyclic phase in the ramp-to-failure phase, the displacement at a 1 N tare load was added to the original measured gage length. To calculate the strain in the ramp-to-failure phase, displacement was divided by the summation of the initial gage length plus the additional accrued length from the cyclic phase (DL/(Linitial ? Ladditional)). Similar to stiffness, the modulus of elasticity was calculated as the linear portion of the stress–strain curve in the failure phase. The percent difference in elongation of the tissue after the cyclic phase of the test was calculated as ((L2000 - L10)/L10) 9 100. The 10th cycle peak was picked to account for initial preconditioning of the tendon. The 2,000th cycle was chosen unless the
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tendon failed in the sub-failure phase. If the specimen failed before the ramp-to-failure phase, the second to last peak was used for calculations as the last cycle would be the load to failure ramp.
(p = 0.139) and cyclic elongation (p = 0.054) exhibited no significant differences between tendon types.
Discussion Statistical analysis Mean and standard deviation were calculated for the maximum load, displacement at maximum load, stiffness, maximum stress, strain at maximum stress, modulus, and cyclic elongation data for each tendon type. A paired t test was conducted to analyze the potential differences between the groups using statistical software (SigmaPlot 12.3; Systat Software, San Jose CA). A difference was considered significant if the calculated p-value was less than a two-tailed a of 0.05.
Results Two Achilles grafts and one quadriceps graft failed during the cyclic testing phase by bone avulsion and were subsequently excluded from analysis. The Achilles specimens failed at cycle number 570 and 993 while the quadriceps specimen failed at cycle number 1,050. All remaining specimens failed during the final ramp-to-failure phase. All specimens failed either by bone avulsion or by a tendon mid-substance rupture, and no slippage or soft tissue failure at the grips was observed during the testing duration. Six of seven Achilles allografts (86 %) failed by bone avulsion and the remaining specimen failed due to mid-substance tendon rupture. Conversely, seven of eight quadriceps allografts (88 %) failed by tendon mid-substance rupture with the other two specimens failing by bone avulsion. Structural properties for the quadriceps and Achilles tendons are summarized in Table 1. No significant differences were detected between tendon types for cross-sectional area (p = 0.721) and maximum load (p = 0.413). Quadriceps grafts had a significantly higher displacement at maximum load (p = 0.040) than Achilles grafts with a 1.09 mm difference between mean values. Quadriceps also had a significantly lower and stiffness (p = 0.029) than Achilles with a difference of 56.16 N/mm. Similarly, material properties for the quadriceps and Achilles tendons are summarized in Table 2. Maximum stress (p = 0.366), strain at maximum stress (p = 0.072), modulus
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Having multiple graft options is advantageous for meeting the steadily increasing demand of ACL-R procedures. Allografts offer an abundant volume of tissue without the complications of donor site morbidity, and advances in donor screening, aseptic processing and terminal sterilization have decreased the risk of disease transmission. Both Achilles and quadriceps tendon allografts offer ample soft tissue with a bone plug for secure fixation, but quadriceps tendon graft use has surprisingly trailed that of Achilles tendon grafts. This direct, biomechanical comparison of quadriceps and Achilles tendon allografts showed no statistically significant differences in six out of eight structural and material properties in an effort to promote quadriceps tendon as a practical graft alternative. Material and structural properties of non-irradiated, fresh frozen quadriceps and Achilles tendons have been reported (Dargel et al. 2006; Harris et al. 1997; Lewis and Shaw 1997; Staubli et al. 1996; Wren et al. 2001). Maximum load to failure is one property of clinical relevance since it represents the tissue’s capacity for resisting and transmitting loads. For quadriceps tendon, our maximum load to failure results (830.14–1797.02 N) were consistent with the range of 131–2353 N (Staubli et al. 1996) cited in the literature. Additionally, our quadriceps tendon allografts exhibited displacements at maximum load of 8.36 ± 0.81 mm and strains at maximum stress of 16 ± 2 % that were comparable to displacements [5.9 ± 1.2 mm (Schatzmann et al. 1998)] and strains [14.7 ± 3.7 % (Staubli et al. 1999)] reported in the literature. For Achilles tendons, our maximum load results (397.49–1349.92 N) overlapped the lower end of the reported range of 843–5194 N (Lewis and Shaw 1997; Wren et al. 2001) and our displacement at maximum load (5.06–15.43 mm) included, but was broader than, the reported range of 1.8–8.7 mm (Lewis and Shaw 1997). Both the quadriceps and the Achilles tendon strain at maximum stress (15.0 ± 7 and 16 ± 2 %, respectively) are consistent with reported ACL strains at maximum stress of 15–19 % (Butler et al. 1986).
Cell Tissue Bank Table 1 Structural properties (mean ± SD) Cross-sectional area (mm2)
Max load (N)
Disp. @ max load (mm)
Stiffness (N/mm)
Achilles tendon
55.2 ± 5.8
915 ± 326
7.57 ± 3.62
217 ± 45
Quadriceps tendon
57.4 ± 14.7
1055 ± 313
8.36 ± 0.81
161 ± 48
p value Significance
0.721 NS
0.413 NS
0.040 Significant
0.029 Significant
Table 2 Material Properties (mean ± SD)
Achilles tendon
Max stress (MPa)
Strain @ max stress (mm/mm)
Modulus (MPa)
Cyclic elongation (%)
16.0 ± 7.32
0.15 ± 0.07
201 ± 70
1.29 ± 0.50 1.97 ± 0.69
Quadriceps tendon
19.1 ± 5.42
0.16 ± 0.02
153 ± 46
p value
0.366
0.072
0.139
0.054
Significance
NS
NS
NS
NS
These differences were likely due to variations in the boundary conditions of our test methodology compared to those in the literature. In an effort to replicate clinically relevant failures, the bone blocks of specimens in this study were potted without constraining the bone-tendon interface to allow for failures such as bone avulsions to occur. Other studies often embedded the bone blocks in castings or metal fixtures to restrain the bone block (Lewis and Shaw 1997; Staubli et al. 1999; Wren et al. 2003), which likely drove failure loads (and corresponding failure stresses) higher by artificially forcing failure paths from the bone-tendon interface to the stronger tendon. Our investigation of cyclic elongation is clinically valuable because it characterized the amount of slack a tendon graft accrues after repeated subfailure loading analogous to some activities of daily living. Quadriceps and Achilles tendons in this study demonstrated similar elongations of 1.97 and 1.29 %, respectively, which corresponded to mean changes of 0.99 and 0.64 mm. Such minimal changes in graft length are important for maintaining the relative anatomic positions of the femur and tibia during postsurgical activities. It is noted that three specimens failed by bone avulsion during the cyclic loading phase and therefore were excluded from the analysis. This exclusion was justified since the resulting elongation could not be attributed solely to the tendon but rather included separation of the bone block and tendon realignment as it rotated to resist the applied tensile force, and failing by
a different strain rate than the load to failure protocol. These premature failures may have been a byproduct of our gripping configuration, which as previously stated made the specimens susceptible to failure by bone avulsion. Displacement at maximum load and stiffness were the only significantly different biomechanical properties observed in this study. The differences may be attributable to contrasts in how each tendon type is attached to their respective bone blocks. The quadriceps tendon attaches to the dense cortical bone of the patella while the Achilles tendon attaches to more porous cancellous bone of the calcaneus. Our observation that quadriceps grafts had only a 12.5 % bone avulsion rate compared to an 86 % avulsion rate for Achilles tendons suggests that the latter abruptly fails at the bone block before it has the ability to reach the same maximum load and having a similar displacement at the maximum load. The larger displacement and lower stiffness observed for quadriceps tendons may indicate that the patella-tendon interface is stronger than that of the Achilles, which thereby shifts the failure initiation to the tendon as supported by the higher occurrences of mid-substance rupture. One limitation of this study was that all specimens were procured from male donors, so any potential gender-based differences could not be examined. This was not intentional as specimens were randomly selected from a pool of research-consented donors, but instead is representative of our tissue bank’s donor population that is historically two-thirds male. We do
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not feel that this is an issue as other studies performed in our laboratory have not shown biomechanical differences in BTB and tibialis allografts due to donor gender (data submitted for publication). Additionally this study is statistically underpowered. Initial study design considered outcomes of previous research and the sample sizes were designed to achieve a power of 0.80. Due to sample size reduction from cyclic load failures and variation in the results a post hoc power analysis indicated an underpowered test. Lack of power is a recognized limitation of this study. This study also only addresses the grafts’ time zero biomechanical properties, which cannot be extrapolated to longer term, clinical graft performance influenced by biologic healing responses. Our testing was conducted on an isolated tendon section rather than the entire tendon. Initial attempts to test whole grafts were unsuccessful due to limitations in our gripping system, and after observing a high incidence of failures caused by the grips we revised our specimen design. The quadriceps tendons proved especially challenging since they are comprised of multiple connected bundles. Our isolation of the central third of the rectus femoris and the vastus intermedius bundles emulated reported clinical procedures for graft preparation (Han et al. 2008a; Santori et al. 2004; West and Harner 2005), and the corresponding Achilles grafts were fashioned in the same manner to produce similar specimens for comparison. Should clinicians choose to utilize all bundles of the quadriceps tendon the increased tissue mass could bolster the graft’s biomechanical capabilities. In conclusion, based on the observed equivalence of biomechanical results and anatomical similarities, our recommendation is that quadriceps tendon allografts are biomechanically equivalent to Achilles tendon allografts when they are both aseptically processed and terminally sterilized with gamma irradiation. A history of positive clinical outcomes for quadriceps tendon autografts in ACL-R also suggests that quadriceps tendon allografts may yield favorable clinical results.
References Belisle A, Bicos J, Geaney L, Anderson M, Obopilwe E, Rincon L et al (2007) Strain pattern comparison of double- and
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singlebundle anterior cruciate ligament reconstruction techniques with the native anterior cruciate ligament. Arthroscopy 23(11):1210–1217 Butler DL, Kay MD, Stouffer DC (1986) Comparison of material properties in fascicle-bone units from human patellar tendon and knee ligaments. J Biomech 19(6):425–432 Dargel J, Schmidt-Wiethoff R, Schneider T, Bruggemann G, Koebke J (2006) Biomechanical testing of quadriceps tendon-patellar bone grafts: an alternative graft source for press-fit anterior cruciate ligament reconstruction? Arch Orthop Trauma Surg 126:265–270 Freedman K, D’Amato M, Nedeff D, Kaz A, Bach B (2003) Arthroscopic anterior cruciate ligament reconstruction: a metaanalysis comparing patellar tendon and hamstring tendon autografts. Am J Sports Med 31(1):2–11 Geib T, Shelton W, Phelps R, Clark L (2009) Anterior cruciate ligament reconstruction using quadriceps tendon autograft: intermediate-term outcome. Arthroscopy 25(12):1408– 1414 Hamner D, Brown C, Steiner M, Hecker A, Hayes W (1999) Hamstring tendon grafts for reconstruction of the anterior cruciate ligament: Biomechanical evaluation of the use of multiple strands and tensioning techniques. J Bone Joint Surg Am 81(A(4)):549–557 Han HS, Seong SC, Lee S, Lee MC (2008a) Anterior cruciate ligament reconstruction. Clin Orthop Relat Res 466:198– 204 Han HS, Seong SC, Lee S, Lee MC (2008b) Anterior cruciate ligament reconstruction : quadriceps versus patellar autograft. Clin Orthop Relat Res 466(1):198–204 Harris L, Smith D, Lamoreaux L, Purnell M (1997) Central quadriceps tendon for anterior cruciate reconstruction. Am J Sports Med 25(1):23–28 Hoburg AT, Keshlaf S, Schmidt T, Smith M, Gohs U, Perka C et al (2010) Effect of electron beam irradiation on biomechanical properties of patellar tendon allografts in anterior cruciate ligament reconstruction. Am J Sports Med 38(6):1134–1140 Howe J, Johnson R, Kaplan M (1991) Anterior cruciate ligament reconstruction using quadriceps patellar tendon graft. Part I: long-term follow up. Am J Sports Med 7:801–811 ISO 11137-2:2006 Sterilization of health care products-radiation-Part 2: establishing the sterilization dose Kaplan M, Howe J, Flemming B, Johnson R, Jarinen M (1991) Anterior cruciate ligament reconstruction using quadriceps patellar tendon graft. Part II: a specific sport review. Am J Sports Med 19(5):458–462 Lewis G, Shaw K (1997) Tensile properties of human tendo Achillis: effect of donor age and strain rate. J Foot Ankle Surg 36(6):435–445 Liu S, Kabo M, Osti L (1995) Biomechanics of two types of Bone-tendon-bone graft for ACL reconstruction. J Bone Joint Surg (Br) 77-B:232–235 Marshall J, Warren R, Wickiewicz T, Reider B (1979) The anterior cruciate ligament: a technique of repair and reconstruction. Clin Orthop 19:458–462 Nicklin S, Waller C, Walker P, Chung W, Walsh W (2000) In vitro structural properties of braided tendon grafts. Am J Sports Med 28(6):790–793 Paessler H, Mastrokalos D (2003) Anterior cruciate ligament reconstruction using semitendinosus and gracilis tendons,
Cell Tissue Bank bone patellar tendon, or quadriceps tendon-graft with press fit fixation without hardware, a new and innovative procedure. Orthop Clin N Am 34:49–64 Santori N, Adriani E, Pederzini L (2004) ACL reconstruction using quadriceps tendon. Orthopedics 27(1):31–35 Schatzmann L, Brunner P, Staubli HU (1998) Effect of cyclic preconditioning on the tensile properties of human quadriceps tendons and patellar ligaments. Knee Surg Sports Traumatol Arthrosc 6(Suppl 1):S56–S61 Scheffler S, Sudkamp N, Gockenjan A, Hoffmann R, Weiler A (2002) Biomechanical comparison of hamstring and patellar tendon graft anterior cruciate ligament reconstruction techniques: the impact of fixation level and fixation method under cyclic loading. Arthroscopy 18(3): 304–315 Schindler A (2012) Surgery for anterior cruciate ligament deficiency: a historical perspective. Knee Surg Sports Traumatol Arthrosc 20:5–47 Shelton W, Fagan B (2001) Autografts commonly used in anterior cruciate ligament reconstruction. J Am Acad Orthop Surg 19(5):259–264 Siebold R, Buelow JU, Bos L, Ellerman A (2003) Primary ACL reconstruction with fresh-frozen patellar versus Achilles tendon allografts. Arch Orthop Trauma Surg 123:180–185
Staubli H, Schatzmann L, Brunner P, Rincon L, Nolte L (1996) Quadriceps tendon and patellar ligament: cryosectional anatomy and structural properties in young adults. Knee Surg Sports Traumatol Arthrosc 4:100–110 Staubli H, Schatzmann L, Brunner P, Rincon L, Nolte L (1999) Mechanical tensile properties of the quadriceps tendon and patellar ligament in young adults. Am J Sports Med 27(1):27–34 Tashman S, Kopf S, Fu F (2008) The kinematic basis of anterior cruciate ligament reconstruction. Oper Tech Sports Med 16(3):116–118 West R, Harner C (2005) Graft Selection in anterior cruciate ligament reconstruction. J Am Acad Orthop Surg 13:197–207 Wren T, Yerby S, Beaupre G, Carter D (2001) Mechanical properties of the human aachilles tendon. Clin Biomech 16:245–251 Wren T, Lindsey D, Beaupre G, Carter D (2003) Effects of creep and cyclic loading on the mechanical properties and failure of human achilles tendon. Ann Biomed Eng 31:710–717
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