Hamstrings Tendons Thickness in ACL Reconstruction: Is it Possible to Predict it By Isometric Torque in Soccer Athletes? Volume 5 - Issue 3

José Martins Juliano Eustaquio¹*, Alberto Martins Fontoura Borges¹, Leandro Pereira de Mendonça¹, Cássio Lucas Dias do Prado¹, Pedro Debieux² and Octávio Barbosa Neto³

• ¹Mário Palmerio Hospital, University of Uberaba (UNIUBE), Orthopedics and Traumatology Group, Brazil.
• ²Hospital Israelita Albert Einstein, Brazil.
• ³Federal University of Triângulo Mineiro (UFTM – Universidade Federal do Triângulo Mineiro, Exercise Science, Health and Human Performance Research Group, Graduate Program in Physical Education, Brazil

Received:July 6, 2021   Published:July 22, 2021

Corresponding author: José Martins Juliano Eustaquio, Mário Palmerio Hospital, University of Uberaba (UNIUBE – Universidade de Uberaba), Department of Orthopedics and Traumatology, Av. Nenê Sabino, n. 2477, Santos Dumont District, Uberaba, Minas Gerais, Brazil

DOI: 10.32474/OSMOAJ.2021.05.000213

 

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Abstract

Objective: To acess the relationship between knee flexor and extensor torques and the thickness of the quadruple hamstrings tendons, extracted during anterior cruciate ligament (ACL) reconstruction surgery, in amateur soccer athletes.
Materials and Methods: This is a cross-sectional study in which 38 amateur soccer athletes of both genders, diagnosed with recent and isolated ACL ligament injury, participated. Epidemiological (gender, age, and dominant limb), anthropometric (height, weight, and BMI), and biomechanical data of the injured lower limb (isometric extensor and flexor torques of the ipsilateral knee) were evaluated. Pearson’s correlation test was used to analyze the correlation of torques with the quantitative variables of the study, and the multivariate analysis was performed using the linear regression test with one-way ANOVA and the calculation of R2. The level of statistical significance was set at 5% (p< 0.05).
Results: The final study sample (33 participants) had a mean age of 30 years, with 81.8% males. Significant correlations were observed between knee flexor torque and height (p=0.002), weight (p=0.01) and graft diameter (p<0.001). In multivariate analysis a statistically significant result was observed for flexor torque (p=0.007).
Conclusion: Knee flexor torque can be tool for preoperative analysis of flexor tendon thickness during surgical programming of knee ligament reconstructions

Keywords: Knee Joint; Anterior Cruciate Ligament Injuries; Soccer; Isometric Contractions

Introduction

The anterior cruciate ligament (ACL) lesion has a high incidence in orthopedic practice [1], especially in young and physically active population [2,3], with an incidence of approximately 85 per 100,000 people aged 16 to 39 years [4,5]. In soccer these injuries are common [5] and occur mainly due to the rotational movements characteristic of the dynamics of the sport, which has also motivated the emergence and use of injury prevention protocols [6]. The treatment of ACL injuries takes into account mainly the current and future functional demands of the patient. However, in most cases, the recommended treatment is surgical [7]. Among the graft options for ACL reconstruction there are allografts and autografts. Allografts are used basically in cases of multiligamentous injuries and successive ACL reconstruction revisions, because it is known to be associated with a higher rate of graft rupture [8]. Among the autografts, the options are the patellar, quadriceps, and hamstrings tendons (gracilis and semitendinosus). Currently, surgeons prefer the hamstrings tendons, which are used in approximately 50% of cases, followed by the patellar and quadriceps tendons [9], the latter with a recent increase in popularity. The total thickness of a graft depends basically on anatomic and biomechanic factors [10,11] and needs a minimum measurement that provides joint stability and survival. In relation to the patellar and quadriceps tendons, the graft corresponds to a fraction of the tendon, which guarantees, therefore, a satisfactory final thickness. However, regard to the hamstring’s tendons, the graft is equivalent to the total volume of the gracilis and semitendinosus tendons, usually in quadruple final shape. This causes, during surgical programming, a greater dependence on knowing this measure more precisely, because it is known that grafts smaller than 08 mm evolve with higher rates of rupture [12]. The evaluation of objective anthropometric and/or biomechanical parameters with good clinical accuracy in the preoperative period would be fundamental to help the surgeon to decide the type of graft to be used. Some works have tried to make this association [13-16], but we still observed low clinical employability. The direct measurement of the biomechanical function of the tendon, through the evaluation of strength using validated instruments, such as the portable isometric dynamometer [17,18], can be an additional tool for this purpose.
The general objective of this study was to evaluate the relationship between torque (using a hand-held isometric dynamometer) of the thigh muscles (flexors and extensors of the knee) and the thickness of the hamstring’s tendons in quadruple format, used as graft in ACL reconstruction surgery, in amateur soccer athletes. The hypothesis was that higher flexor and extensor torques of the knee are associated with greater thickness of the flexor tendons.

Materials and Methods

This is an observational, cross-sectional study, in which amateur soccer athletes (minimum practice of three times/week) from a city in the interior of the State of Minas Gerais (Brazil), of both genders, with diagnosis of recent ACL injury participated. The study was approved by the Research Ethics Committee of the University of Uberaba (CAAE n°. 97858718.6.0000.5145). All participants signed the Informed Consent Form.
Inclusion criteria were amateur soccer athletes of both genders, aged between 18 and 50 years, with primary and isolated ACL ligament injury (based on clinical history, physical examination and confirmed by magnetic resonance imaging and/ or arthroscopy procedure) with indication for surgical treatment. The exclusion criteria were for those with posterior thigh muscle injury, ACL rupture more than 6 months after surgery, ACL injury that occurred outside the sports environment, previous intrinsic knee injury (ligament, meniscal or chondral), chronic and limiting knee pain without confirmed diagnosis, current injury of another knee ligament complex besides the ACL and histories of fracture and surgery that occurred previously, all these criteria related to the lower limb and/or knee ipsilateral to the ACL injury. The sample was selected by convenience, as it was a limited public, with strict inclusion and exclusion criteria used to reduce information bias during biomechanical assessment of the injured limb. This selection occurred during 14 months after the study was accepted by the Research Ethics Committee of the University of Uberaba.

Procedure

In the preoperative period, epidemiological (gender, age, and dominant limb), anthropometric (height, weight, and BMI) data were evaluated using an electronic scale (Welmy, W200A), and biomechanical data of the injured lower limb (isometric extensor and flexor torques of the ipsilateral knee). The knee torques were performed with a portable dynamometer (Lafayette Instrument, Model 01165, USA), positioned perpendicular to the body surface and through which the peak force was evaluated. The dynamometer support point was standardized, and the lever arm was calculated by the distance, in meters, between this point and the center of the knee joint, using a flexible anthropometric tape measure (Sanny®). A specific angulation of the knee was defined to perform the tests, optimized according to the length x tension curve of the muscle group evaluated [19,20], with confirmation using a goniometer (Sanny®).
The test to evaluate the isometric strength of the flexors was performed with the knee in 60º position and the dynamometer positioned posteriorly in the calcaneal region, five centimeters from the medial malleolus [21,22] (Figure 1). For extensor assessment, the dynamometer was positioned in the anterior region of the distal third of the tibia, also five centimeters proximal to the medial malleolus, with the knee flexed at 60º [21,22] (Figure 1). The device was stabilized by the examiner’s hand and fixed with the help of a rigid belt, which eliminated measurement bias due to the force exerted by the examiner.
As a warm-up before the tests, we initially requested a submaximal isometric contraction for each muscle group to familiarize them with the procedure and the equipment. After this process, three maximum isometric contractions were requested, with continuous verbal stimulation from the examiner, and the average strength between the three measurements was considered for analysis. The duration of each contraction was standardized in five seconds, followed by 30 seconds’ rest. The data were recorded in Newtons (N). The tests were performed by the same examiner. The torque, which is the biomechanical variable of choice for the study of joint forces, was calculated by the product between the average of the three maximum forces (both knee extension and flexion) and the lever arm of the knee, with the result established in N/m.
The surgical technique was performed in a standardized way by the same surgeon, who is a specialist in Knee Surgery and a full member of the Brazilian Knee Surgery Society. The first stage of the ACL reconstruction surgery is based on the removal of the tendon graft, which in this study were the gracilis and semitendinosus tendons. This procedure was performed through a vertical incision of approximately 2 cm on the anteromedial side of the proximal tibia (Figure 2).
The tendons were prepared on a surgical table (Figure 3), with removal of the muscle remnants, and then the thickness of their quadruple shape was measured through a standardized guide (Figure 4), whose holes have graduations every 05 mm. The thickness was defined as the value following the measure in which the quadruple graft was not able to cross longitudinally the hole of the guide.

Statistical analysis

Data were processed in Excel® and SigmaStat®2.0 software (GraphPad Software Jandel, SPSS, Chicago, IL, USA). The Kolmogorov-Smirnov test was used to verify the normality of the data distribution. Continuous variables with normal distribution were presented as mean and standard deviation. The results were organized in tables.
Student’s t-test was used to compare quantitative variables regarding flexor and extensor torques according to gender. Pearson’s correlation test was used to analyze the correlation of the torques with the quantitative variables of the study, and the multivariate analysis was performed using the linear regression test with the ANOVA one-way test and the calculation of R2. The linear regression test was also used for the prediction of a formula for preoperative estimation of the diameter of flexor tendon grafts. The level of statistical significance was set at 5% (p < 0.05).

Results

The study was attended by 38 amateur field soccer athletes. The exclusion rate was 13% (Figure 5).
The study variables showed low variability coefficient, therefore classified as homogeneous data. In the flexor torque analysis, the male athletes presented means with statistically significant values in relation to the female athletes (Table 2). Significant correlations were observed between knee flexor torque and the height (p=0.002) and weight (p=0.011) of the participants and also with the graft diameter (p<0.001) (Table 3 and Figure 6).

In the multivariate analysis, through the linear regression between the flexor and extension torques and the study variables, statistically significant results were observed for the flexor torque (p=0.007), but without statistical significance of the predictive variables (Table 4). The best statistical model to predict the diameter of the quadruple graft was from the flexor torque (Table 5), and with this the following equation was developed:

Graft Diameter= 6.57 + (0.01 x Flexor Torque)

Discussion

The main finding of this study was the positive and statistically significant correlation between flexor tendon graft thickness and isometric knee flexor torque in amateur soccer athletes. Through this finding, this physical valence can be used as a parameter to estimate the diameter of the hamstring’s tendons in knee ligament reconstructions surgeries. In soccer players, regardless of their performance level, the standard treatment for ACL injuries is surgery. In this public, the choice of the most appropriate graft remains controversial [23,24]. The existing consensus is that the use of allografts should be avoided [25]. The use of hamstrings tendons grafts, despite potentially causing knee flexion strength deficit in specific tests [26,27] and also presenting biomechanical disadvantages compared to bone/tendon grafts [28], is the preferred graft for surgeons in practitioners of this sport [23,29].
Besides hamstrings tendons being one of the main autograft options, in some situations they are also the priority of choice [30,31], provided they present minimum diameters that guarantee stability in the postoperative period. It is known that grafts in ACL reconstruction surgery with diameters less than or equal to 8 mm are associated with higher rates of rerruptures [32]. For this reason, different techniques have been developed to compensate intraoperatively the unsatisfactory thickness of flexor tendons, such as intrinsic adaptations to transform them into fivefold and sixfold formats [33,34], solidarization with autografts or allografts (hybrid graft) [35], and more recently, the preservation of muscle remnants [36].
However, in some situations it is not possible to perform these techniques, mainly when there is a scarcity of adequate instruments or anatomic limitations of the graft itself. For reasons of this nature, it is prudent that the knee surgeon has at hand, in a practical and reproducible way and prior to surgery, tools that provide a guarantee of the average thickness of the flexor tendons. However, up to now, there is no objective and commonly used method in clinical practice to guide the surgeon in estimating the thickness of the hamstring’s tendons preoperatively. Some imaging tests have been studied with this objective [15,16]. Nuclear magnetic resonance (NMR), considered the gold standard in diagnosing ACL injury, can be used as an auxiliary measure in the preoperative evaluation of tendon diameter. For this, one of the criteria with good clinical accuracy is the measurement of tendon thickness at its greatest diameter in the axial plane, with the medial epicondyle of the femur as an anatomical reference [15]. Another possible imaging method is ultrasonography (USG), which can be performed based on anteroposterior and transverse diameters (measured in mm) and cross-sectional area (mm²) [13,14]. However, unlike MRI, USG is not a test of choice for the patient with knee ligament injury and, in this case, would be performed only for the purpose of assessing the thickness of the hamstring’s tendons. Moreover, the results of USG with this purpose present conflicting results in the literature [13,14] and, so far, it is not routinely used.
The relationship between epidemiological and anthropometric parameters of easy practical execution, such as gender, age, weight, height, lower limb length, body mass index, among others, and hamstrings tendons thickness have also been studied [10,11,37,38]. However, among all these parameters, height is the only factor that presents a significant association and reproducible results [37,38], as observed in the current study, in which height presented a positive and significant correlation with flexor torque. As it is an easily evaluated parameter, even in a hospital environment, it should be evaluated preoperatively as one of the ways to consider the choice of graft in ACL reconstruction.
It is known that a physical training program with musculoskeletal demands like soccer, based on aerobic and anaerobic overloads, leads to gains not only in strength and muscle hypertrophy of the segments worked, but also in hypertrophy of the tendinous unit, but at a lower intensity [39-41]. This data from the literature justifies the finding of a significant correlation between graft thickness and knee flexor torque observed in the current study. Moreover, it is a factor that corroborates the use of this biomechanical resource as an adjuvant measure to predict the diameter of hamstrings tendons in active populations.In this study, whose main objective was to analyze the efficacy of a practical and additional resource to analyze hamstrings tendons thickness in a specific population, we used the isometric hand-held dynamometer, which is a tool well validated in the literature for strength analysis [17,18,22] and has a much lower cost than the isokinetic dynamometer.
The main precautions that must be taken when using this portable instrument are the standardization of the test time, the adequate positioning in the limb, the use of rigid belts, and joint angulation. Of these, the biomechanical importance of defining the lever arm, which is the measurement that will provide the calculation of torque and whose size can change the peak force produced, and the joint angulation, which should be optimized according to the length x tension curve of the muscle grouping analyzed, must be emphasized [19,20].
The main limitations of the study were its cross-sectional design and gender bias, still common in studies with soccer players [42,43]. Another limiting factor was the non-blinding of the evaluators regarding the graft thickness because the procedure was always performed and recorded by the surgeon and the same evaluator. Moreover, the measurement of the graft thickness was not performed continuously, but by intervals of 0.5 mm according to the standardization of the specific guide. Further research with this theme, in different populations, will be important for future comparisons with the findings of the current study, as it is suggested that soccer athletes have higher flexion and extension torques of the knee in relation to the population in general.

Conclusion

Associated with the analysis of anthropometric characteristics, especially the patient’s height, knee flexor torque can be another tool for preoperative analysis of hamstrings tendons thickness during the surgical programming of ACL reconstruction.

References

1. Mall NA, Chalmers PN, Moric M, Tanaka MJ, Cole BJ, et.al. (2014) Incidence and trends of anterior cruciate ligament reconstruction in the United States. Am J Sports Med 42(10): 2363-2370.
2. Bram JT, Magee LC, Mehta NN, Patel NM, Ganley TJ, et.al. (2021) Anterior Cruciate Ligament Injury Incidence in Adolescent Athletes: A Systematic Review and Meta-analysis. The American Journal of Sports Medicine 49(7): 1962-1972.
3. Beck NA, Lawrence JTR, Nordin JD, DeFor TA, Tompkins M et.al. (2017) ACL tears in school-aged children and adolescents over 20 years. Pediatrics 139(3): e20161877.
4. Lynch TS, Parker RD, Patel RM, Andrish JT; MOON Group, Spindler KP, et.al. (2015) The Impact of the Multicenter Orthopaedic Outcomes Network (MOON) Research on Anterior Cruciate Ligament Reconstruction and Orthopaedic Practice. J Am Acad Orthop Surg 23(3): 154-163.
5. Kaeding CC, Léger-St-Jean B, Magnussen RA (2017) Epidemiology and Diagnosis of Anterior Cruciate Ligament Injuries. Clin Sports Med 36(1): 1-8.
6. Silvers-Granelli HJ, Bizzini M, Arundale A, Mandelbaum BR, Snyder-Mackler L, et.al. (2017) Does the FIFA 11+ Injury Prevention Program Reduce the Incidence of ACL Injury in Male Soccer Players? Clin Orthop Relat Res 475(10): 2447-2455.
7. Diermeier T, Rothrauff BB, Engebretsen L, Lynch AD, Ayeni OR, (2020) Treatment after anterior cruciate ligament injury: Panther Symposium ACL Treatment Consensus Group. Knee Surg Sports Traumatol Arthrosc 28(8): 2390-2402.
8. Magnussen RA, Lawrence JT, West RL, Toth AP, Taylor DC, et.al. (2012) Graft size and patient age are predictors of early revision after anterior cruciate ligament reconstruction with hamstring autograft. Arthroscopy 28(4): 526-531.
9. Barrett GR, Luber K, Replogle W, Manley Jl (2010) Allograft anterior cruciate ligament reconstruction in the young, active patient: tegner activity level and failure rate. Arthroscopy 26(12): 1593-1601.
10. Arnold MP, Calcei JG, Vogel N, Magnussen RA, Clatworthy M, et.al. (2021) ACL Study Group survey reveals the evolution of anterior cruciate ligament reconstruction graft choice over the past three decades. Knee Surg Sports Traumatol Arthrosc.
11. Ho SWL, Tan TJL, Lee KT (2016) Role of anthropometric data in the prediction of 4-stranded hamstring graft size in anterior cruciate ligament reconstruction. Acta Orthop Belg 82: 72-77.
12. Goyal S, Matias N, Pandey V, Acharya K (2016) Are pre-operative anthropometric parameters helpful in predicting length and thickness of quadrupled hamstring graft for ACL reconstruction in adults? A prospective study and literature review. Int Orthop 40(1): 173-181.
13. Takenaga T, Yoshida M, Albers M, Nagai K, Nakamura T, et.al. (2019) Preoperative sonographic measurement can accurately predict quadrupled hamstring tendon graft diameter for AC reconstruction. Knee Surg Sports Traumatol Arthrosc 27(3): 797-804.
14. Astur DC, Novaretti JV, Liggieri AC, Janovsky C, Nicolini AP, et.al. (2018) Ultrassonografia para avaliação do diâmetro dos tendões flexores do joelho: é possível predizer o tamanho do enxerto? Rev Bras Ortop 53(4): 404-409.
15. Kupczik F, Tauscheck LOB, Schiavon MEG, Sbrissia B, Ernlund LSR, et.al. (2016) Predição do diâmetro do enxerto dos tendões flexores na reconstrução do ligamento cruzado anterior por meio da ressonância nuclear magné Rev Bras Ortop 51(4): 405-411.
16. Camarda L, Grassedonio E, Albano D, Galia M, Midiri M, et.al. (2018) MRI evaluation to predict tendon size for knee ligament reconstruction. Muscles Ligaments Tendons J 7(3): 478-484.
17. Whiteley R, Jacobsen P, Prior S, Skazalski C, Otten R, et.al. (2012) Correlation of isokinetic and novel hand-held dynamometry measures of knee flexion and extension strength testing. J Sci Med Sport 15(5): 444-450.
18. Jackson SM, Cheng MS, Smith AR Jr, Kolber MJ (2017) Intrarater reliability of handheld dynamometry in measuring lower extremity isometric strength using a portable stabilization device. Musculoskelet Sci Pract 27: 137-141.
19. Noorkoiv M, Nosaka K, Blazevich AJ (2014) Neuromuscular adaptations associated with knee joint angle-specific force change. Med Sci Sports Exerc 46(8): 1525-1537.
20. Alegre LM, Ferri-Morales A, Rodriguez-Casares R, Aguado X (2014) Effects of isometric training on the knee extensor moment-angle relationship and vastus lateralis muscle architecture. Eur J Appl Physiol 114(11): 2437-2446.
21. Jackson SM, Cheng MS, Smith AR Jr, Kolber MJ (2017) Intrarater reliability of handheld dynamometry in measuring lower extremity isometric strength using a portable stabilization device. Musculoskelet Sci Pract 27: 137-141.
22. Mentiplay BF, Perraton LG, Bower KJ, Adair B, Pua YH, et.al. (2015) Assessment of Lower Limb Muscle Strength and Power Using Hand-Held and Fixed Dynamometry: A Reliability and Validity PloS One 10(10): e0140822.
23. Martin-Alguacil JL, Arroyo-Morales M, Martín-Gomez JL, Monje-Cabrera IM, Abellán-Guillén JF, (2018) Strength recovery after anterior cruciate ligament reconstruction with quadriceps tendon versus hamstring tendon autografts in soccer players: A randomized controlled trial. Knee 25(4): 704-714.
24. Britt E, Ouillette R, Edmonds E, Chambers H, Johnson K, et.al. (2020) The Challenges of Treating Female Soccer Players with ACL Injuries: Hamstring Versus Bone-Patellar Tendon-Bone Autograft. Orthop J Sports Med 8(11): 2325967120964884.
25. Kaeding CC, Pedroza AD, Reinke EK, Huston LJ (2015) Risk factors and predictors of subsequent ACL injury in either knee after ACL reconstruction: prospective analysis of 2488 primary ACL reconstructions from the MOON cohort. Am J Sports Med 43(7): 1583-1590.
26. Ardern CL, Webster KE, Taylor NF, Feller JÁ (2010) Hamstring strength recovery after hamstring tendon harvest for anterior cruciate ligament reconstruction: a comparison between graft types. Arthroscopy 26(4): 462- 469.
27. Maletis GB, Inacio MC, Funahashi TT (2015) Risk factors associated with revision and contralateral anterior cruciate ligament reconstructions in the Kaiser Permanente ACLR registry. Am J Sports Med 43(3): 641- 647.
28. Reinhardt KR, Hetsroni I, Marx RG (2010) Graft selection for anterior cruciate ligament reconstruction: a level I systematic review comparing failure rates and functional outcome. Orthop Clin N Am 41(2): 249- 262.
29. Arliani GG, Pereira VL, Leão RG, Lara PS, Ejnisman B, et.al. (2019) Treatment of Anterior Cruciate Ligament Injuries in Professional Soccer Players by Orthopedic Surgeons. Rev Bras Ortop (Sao Paulo) 54(6): 703-708.
30. Chen H, Liu H, Chen L (2020) Patellar Tendon Versus 4-Strand Semitendinosus and Gracilis Autografts for Anterior Cruciate Ligament Reconstruction: A Meta-analysis of Randomized Controlled Trials with Mid- to Long-Term Follow-Up. Arthroscopy 36(8): 2279-2291.e8
31. Duchman KR, Lynch TS, Spindler KP (2017) Graft Selection in Anterior Cruciate Ligament Surgery: Who gets What and Why? Clin Sports Med 36(1): 25-33.
32. Conte EJ, Hyatt AE, Gatt CJ Jr, Dhawan A (2014) Hamstring autograft size can be predicted and is a potential risk factor for anterior cruciate ligament reconstruction failure. Arthroscopy 30(7): 882-890.
33. Nazari G, Barton KI, Bryant D, Getgood A, Brown CH Jr, et.al. (2020) Five- and six-strand hamstring grafts consistently produce appropriate graft diameters for anterior cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc.
34. Brown CH Jr (2018) Editorial Commentary: How to Increase Hamstring Tendon Graft Size for Anterior Cruciate Ligament Reconstruction. Arthroscopy 34(9): 2641-2646.
35. Kang H, Dong C, Wang F (2019) Small hamstring autograft is defined by a cut-off diameter of 7 mm and not recommended with allograft augmentation in single-bundle ACL reconstruction. Knee Surg Sports Traumatol Arthrosc 27(11): 3650-3659.
36. Funchal LFZ, Ortiz R, Jimenez A, Funchal GDG, Cohen M, et.al. (2021) Remnant Muscle Preservation on Hamstring Tendon Autograft During ACL Reconstruction Promotes Volumetric Increase with Biological and Regenerative Potential. Orthopaedic Journal of Sports Medicine 9(3): 232596712199001.
37. Pinheiro LF Jr, de Andrade MA, Teixeira LE, Bicalho LA, Lemos WG, et.al. (2011) Intra-operative four-stranded hamstring tendon graft diameter evaluation. Knee Surg Sports Traumatol Arthrosc 19(5): 811-815.
38. Janssen RPA, Maria JF, Velden MJFV, Besselaar MV, Reijman M (2017) Prediction of length and diameter of hamstring tendon autografts for knee ligament surgery in Caucasians. Knee Surg Sports Traumatol Arthrosc 25(4): 1199-1204.
39. Seynnes OR, Erskine RM, Maganaris CN, Longo S, Simoneau EM, et.al. (2009) Training-induced changes in structural and mechanical properties of the patellar tendon are related to muscle hypertrophy but not to strength gains. J Appl Physiol 107(2): 523-530.
40. Magnusson SP, Hansen P, Kjaer M (2003) Tendon properties in relation to muscular activity and physical training. Scand J Med Sci Sports 13(4): 211-223.
41. Reggiani C, Schiaffino S (2020) Muscle hypertrophy and muscle strength: dependent or independent variables? A provocative review. Eur J Transl Myol 30(3): 9311.
42. Marom N, Dooley MS, Burger JA, Chang B, Coleman SH, et.al. (2020) Characteristics of Soccer Players Undergoing Primary Hip Arthroscopy for Femoroacetabular Impingement: A Sex- and Competitive Level–Specific Analysis. The American Journal of Sports Medicine 48(13): 3255-3264.
43. Larruskain J, Lekue JA, Diaz N, Odriozola A, Gil SM (2018) A comparison of injuries in elite male and female football players: A five-season prospective study. Scand J Med Sci Sports 28(1): 237-245.