Knee Surgery, Sports Traumatology, Arthroscopy https://doi.org/10.1007/s00167-018-5265-z

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Anatomy of proximal attachment, course, and innervation of muscles: a pictorial essay

Karolina Stępień1 · Robert Śmigielski2,3 · Caroline Mouton4 · Bogdan Ciszek5,6 · Martin Engelhardt7 · Romain Seil4,8

Received: 12 July 2018 / Accepted: 23 October 2018 © European Society of Sports Traumatology, Surgery, Arthroscopy (ESSKA) 2018

Abstract Hamstring injuries are very common in sports medicine. Knowing their anatomy, morphology, innervation, and function is important to provide a proper diagnosis, treatment as well as appropriate prevention strategies. In this pictorial essay, based on anatomical dissection, the detailed anatomy of muscle–tendon complex is reviewed, including their proximal attachment, muscle course, and innervation. To illustrate ’ role in the rotational control of the , the essay also includes the analysis of their biomechanical function. Level of evidence V (expert opinion based on laboratory study).

Keywords Hamstring · Hamstring anatomy · Hamstring injury · Muscle · Biceps femoris · Semimembranosus · Semitendinosus · Posterior · Sciatic

Introduction and skiing [3, 4], but can be observed in the general non- sporting population as well [50]. Males and professional Hamstring injuries are one of the most common prob- football players are particularly at risk of hamstring inju- lems in sports medicine. Their prevalence is estimated to ries [4, 50], which cause on average more than 14 days reach 12–15% among professional football players [22, of time loss from sports participation (range 1–128 days) 28, 87] and increases by 4% annually in this group [31]. It [29]. Although different prevention programs have been is also a major problem of track and field sports, dancing developed, the reinjury risk remains unacceptably high (12–63%). The majority of reinjuries occur at the same location of the hamstrings complex than the primary Electronic supplementary material The online version of this article (https​://doi.org/10.1007/s0016​7-018-5265-z) contains supplementary material, which is available to authorized users.

* Karolina Stępień 3 MIBO Foundation-The International Institute for Orthopaedic [email protected] Research, Twarda 4, 00‑105 Warsaw, Poland Robert Śmigielski 4 Department of Orthopaedic Surgery, Centre Hospitalier [email protected] Luxembourg, Clinique d’Eich. 78, rue d’Eich, 1460 Luxembourg, Luxembourg Caroline Mouton [email protected] 5 Department of Descriptive and Clinical Anatomy, Centre of Biostructure Research, Medical University of Warsaw, Bogdan Ciszek Chałubińskiego 5, 02‑004 Warsaw, Poland [email protected] 6 Department of Neurosurgery, Prof. Bogdanowicz Children Martin Engelhardt Hospital, Niekłańska 4/24, 03‑924 Warsaw, Poland [email protected] 7 Department of Orthopaedics, Trauma and Hand Surgery, Romain Seil Osnabrück Clinic, Am Finkenhügel 1, 49076 Osnabrück, [email protected] Germany 1 Department of Orthopedics, Carolina Medical Center, Pory 8 Sports Medicine Research Laboratory, Luxembourg Institute 78, 02‑757 Warsaw, Poland of Health, 78 rue d’Eich, 1460 Luxembourg, Luxembourg 2 Mirai Institute, Wolska 96, 01‑126 Warsaw, Poland

Vol.:(0123456789)1 3 Knee Surgery, Sports Traumatology, Arthroscopy injury [33, 52, 81, 85]. The common mechanisms of injury the complex was also analysed to bring a fresh perspective are indirect trauma, running and stretching [34]. on this problematic anatomic entity of lower leg. Most of the injuries in football and athletics occur in the midportion of the hamstring muscle–tendon complex [21, The proximal attachment of the hamstrings 30]. Avulsions of the proximal attachment area differ from the above. They have a different injury mechanism and are The semitendinosus (ST), long head of the biceps femo- often caused by a forced hyperextension [7, 8, 16, 20]. ris (long head, lhBF) and semimembranosus (SM) muscles Hamstring tendons are also among the most frequently originate from the (Fig. 1a, b). The ST and harvested grafts for ligament reconstructions. Even though lhBF have a common origin on the posteromedial aspect of they have a high capacity for regeneration [73], functional the ischial tuberosity, over its top. Tendons of the ST and deficits after hamstring tendon harvesting remain common. lhBF are conjoined at a distance of 9.1–10 cm [35, 37, 58, It may induce a reduction of knee flexion, extension and 81]. The SM origin is separate from the previous one and internal rotation [44, 74]. it is located anterolaterally from the ST/lhBF attachment. Recent biomechanical investigations have suggested Fibres of the proximal SM attachment are twisted before that the hamstring muscle–tendon complex plays an forming a proper tendon (Figs. 2a, b, 3a, b, 4). important role in controlling the rotational stability of the A majority of authors agree with the presence of a con- knee. Ultimately, they also play a role in the prevention of joined tendon of the ST/lhBF, but the precise description of the valgus collapse observed in severe knee injuries such its attachment area varies amongst authors. Most of authors as the anterior cruciate ligament (ACL) injuries. Indeed, observed the attachment on the posteromedial aspect of the hamstrings turn out to be the main ACL agonists and pro- ischial tuberosity as in our dissection [61, 68, 82], whereas tectors of the ACL [89, 90]. others indicated it to be directly medial [10, 58] or lateral on A better understanding of the anatomy of the hamstring the ischial tuberosity [35, 60]. Consequently, the SM attach- muscle complex may help to provide a better diagnosis, ment is also described in different ways: on the anterolateral treatment as well as appropriate prevention strategies. The aspect of the ischial tuberosity as in our dissection [61, 68, aim of this article, based on anatomical dissection, was to 82, 84], but also anteriorly [35] or purely lateral [58]. provide a detailed review of the anatomy of muscle–ten- We observed the shape of the ST/lhBF attachment as don complex, including their proximal attachment, muscle being oval and of the SM footprint as a crescent-shaped course, and innervation. This kind of essay with clear and being wider than the ST/lhBF—similar to most of the useful photographic documentation has not been reported authors [58, 61, 68, 82]. in the literature previously. The biomechanical function of The ischial tuberosity is also the area of the distal attach- ment of a (STL)—an elastic and

Fig. 1 a, b Posterior view of the gluteal region and the proximal part of the posterior thigh of a right lower extremity. (1) muscle; (2) ; (3) ischial tuberosity; (4) ; (5) perineal branches of the posterior femoral cutaneous nerve

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dynamic structure [40, 83]. Fibres of the STL are descend- ing from the sacrum to the ischial tuberosity in continuity with fibres of the lhBF [12, 58, 68] (Fig. 5). In the proximal hamstring attachment area, two main bur- sas can be identified. The bursa of the ischial tuberosity cov- ers a prominent part of the ischiatic bone [24, 38, 57]. The bursa of the proximal biceps femoris can be found between the common attachment of the ST/lhBF and the SM fill- ing the space between proximal tendons close to their bony attachment [14](Figs. 6, 7a–c). The proximal attachment of short head of biceps femo- ris (shBF) arises on the middle third of . Its origin is located on the lateral lip of the linea aspera, descending distally and laterally [17].

Course of the muscles

Semitendinosus muscle

The semitendinosus muscle (ST) lies in the posteromedial area of the thigh. It runs distally and medially from its proxi- mal insertion on the ischial tuberosity and lies directly on the SM. From its origin, the ST creates a conjoined tendon with the lhBF forming an . The muscle belly of the ST is fusiform (from external aspect) and has a characteristic oblique or V-shaped raphe (tendinous inscription) [41, 43, Fig. 2 a, b Posterolateral view of the area of the proximal attach- 51, 82, 86]. The distal tendon starts below the mid-thigh ment of the hamstring muscles (right lower extremity). (1) Area of and runs around the medial condyle of the tibia to its distal the attachment of the conjoined tendon of the semitendinosus and the insertion as a part of (Fig. 8). long head of the biceps femoris; (2) the proximal attachment area of the conjoined tendon; (3) conjoined tendon of the semitendinosus and Semimembranosus muscle the long head of the biceps femoris—cut and rotated 180°; (4) proxi- mal tendon of the semimembranosus muscle; (5) area of the attach- ment of the semimembranosus muscle; arrowheads—shape of the The semimembranosus muscle (SM) lies posteromedially in semimembranosus attachment the thigh and has a similar location as the ST. It starts on the

Fig. 3 Proximal tendons of the hamstring muscles—dorsal (a) and abdominal (b) view with indicated direction of the fibres (lines: ST—blue, lhBF—red, SM—white). (1) The conjoined tendon of the semitendinosus and the long head of the biceps femoris; (2) the proximal tendon of the semimembranosus muscle

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Fig. 4 Posterolateral view on the area of the proximal attachment of Fig. 6 Lateral view of the area of the ischial tuberosity (right lower the hamstring muscles. (1) Area of the attachment of conjoined ten- extremity). (1) Sacrotuberous ligament; (2) superficial bursa of the don of the semitendinosus and the long head of the biceps femoris; ischial tuberosity; (3) tendon of the long head of the biceps femoris; (2) area of the attachment of the semimembranosus muscle; (3) quad- (4) sciatic nerve; (5) perineal branches of the posterior femoral cuta- ratus femoris muscle neous nerve; (6) nerve branch to the bursa of the ischial tuberosity

and distal tendons of the lhBF are overlapping [82]. The shBF originates in the posterolateral region of the femur. It fuses with the lhBF in the distal part of the thigh, forming an aponeurotic structure. The conjoined distal tendon of both heads attaches to the head of the fibula [76, 78]. Mean lengths of hamstring muscles according to different authors are shown in Table 1 [42, 82, 85].

Innervation

The sciatic nerve innervates the hamstring muscle complex. The ST, SM, lhBF are innervated through its tibial divi- sion, while the shBF is innervated by its fibular division. The extra-pelvic part of the sciatic nerve appears beyond Fig. 5 Posterior view of the area of the ischial tuberosity (right lower the greater sciatic foramen just under the . extremity). (1) Sacrotuberous ligament; (2) ischial tuberosity; (3) gemellus superior, obturator internus, gemellus inferior muscles; (4) It runs caudally and medially to the ischial tuberosity [66]. piriformis muscle; (5) sciatic nerve; (6) semitendinosus muscle The SM, lhBF, and shBF are supplied by one motor branch, while the ST receives two motor branches from the sciatic nerve, which is running directly to the anterolateral part of the ischial tuberosity to the medial con- [2, 5, 64, 65, 71, 86]. dyle of the proximal tibia to the pes anserinus and descends In the proximal area of the posterior thigh, the sciatic under the ST, from its wide proximal insertion [11]. The nerve gives the motor branch to the lhBF. It contains a few proximal and distal tendons of SM overlap. It means that the terminal branches heading distally and one recurrent which part of fibres in the middle of SM has a connection to both goes directly to the area of the bone attachment of conjoined tendons: the proximal and the distal [82] (Figs. 9, 10a, b). tendon lhBF/ST [54]. The primary motor branch for the ST is located at a similar level as the branch for the lhBF. The secondary motor branch for the ST for the part of the muscle under the raphe and motor branches for the SM and shBF are The biceps femoris muscle (BF) forms the posterolateral located in the distal area of the posterior thigh [5, 64, 65, 71, part of the thigh. It consists of two heads: the long (lhBF) 80, 86] (Figs. 11, 12a–c, 13a, b). and the short head of the biceps femoris (shBF). The proxi- The precise measurements of the entries of the motor mal tendon of the lhBF runs laterally after division of the branches to the hamstring muscles are represented in Table 2 conjoined tendon with the ST. Like in the SM, the proximal [5, 64, 65, 86].

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Fig. 8 Posterolateral view of the posterior thigh of a right leg. (1) Ischial tuberosity; (2) conjoined tendon of the semitendinosus and the log head of the biceps femoris; (3) sciatic nerve; (4) semitendinosus muscle; (5) long head of the biceps femoris muscle

Fig. 7 a–c Lateral view of the area of the proximal attachment of the hamstring muscles (right lower extremity). (1) Ischial tuberosity; (2) conjoined tendon of the semitendinosus and the long head of the biceps femoris; (3) proximal tendon of the semimembranosus muscle; Fig. 9 The hamstring complex. (1) Proximal tendon of the semimem- (4) bursa of the proximal biceps femoris between split tendons branosus muscle; (2) distal tendon of the semimembranosus muscle (3) conjoined tendon of the semitendinosus and the long head of the biceps femoris; (4) tendinous inscription (raphe) of the semitendino- sus muscle; (5) distal tendon of the semitendinosus muscle; (6) com- mon distal tendon of the long and short head of the biceps femoris Biomechanical function of hamstring muscles muscle

The hamstring muscle complex has a major significance in the human kinematic chain, directly influencing the func- posture. The particularity of the hamstrings resides in tion of the lower limb and supporting an upright body the fact that their function can be considered both as a

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simultaneous contraction of hamstring muscles influences both the knee and the so their function cannot be limited to one joint only [46]. Most of hamstring activity as a group is eccentric. During the gait cycle, the hamstrings play a main role in the swing phase. By contraction, they coordinate hip exten- sion and prevent excessive extension of the knee. In the ter- minal swing phase, they also performed a significant amount of negative work (energy absorption) [19, 69]. The hamstring muscles are the main antagonist for the quadriceps femoris muscle (QF). Their coactivation during the contraction of the QF balances the lower limb [32, 35, 88]. At the same time, the hamstring muscles work along- side with the anterior cruciate ligament (ACL) decelerating forward translation of the tibia during knee extension (ACL- agonist muscles) [13, 36, 45, 55, 75, 89, 90]. Through their proximal attachment on the ischial tuber- osity, the hamstrings muscles have a direct influence on the position of the . Posture can be influenced by the forces carried by the STB between the vertebral column and legs which may change the angle of the pelvic axis [83].

Individual function of hamstring muscles

The biomechanical analysis of hamstrings indicates some differences between each of the individual muscles. Based Fig. 10 a, b Posterolateral view of the posterior thigh of a right lower on their anatomy, each muscle generates contractions in a extremity. (1) Conjoined tendon of the semitendinosus and the long slightly different plane and direction. The main results— head of the biceps femoris; (2) ischial tuberosity; (3) proximal tendon knee flexion and hip extension—are the net force of these of the semimembranosus muscle; (4) semimembranosus muscle; (5) components. Analysis prove that the biomechanical load, the semitendinosus muscle; (6) long head of the biceps femoris muscle; (7) short head of the biceps femoris muscle; (8) conjoined tendon of metabolic activity, and the EMG activity of each hamstring the long and the short head of the biceps femoris muscle differ [66, 69, 70, 89]. The BF with its distal insertion on the lateral side of the proximal fibula and tibia influences stability of the poste- synergistic work of the entire muscle group, but also indi- rolateral corner of the knee [77]. The contraction of the BF vidually for each muscle. rotates the tibia and fibula externally [56, 75, 77]. Conse- quently, it prevents internal rotation of the tibia in relation to Hamstring muscles functioning as a group the femur [9]. The BF is the most effective hamstring muscle in reducing the ACL-loading component produced by the The primary functions of the hamstring muscles, aris- QF through decreasing anterior tibial translation [13, 25]. ing from their biarticular arrangement, are knee flexion, Due to their distal insertion on the medial part of the hip extension and slight abduction of the lower limb. The proximal tibia, the ST and SM contraction induce an internal

Table 1 Mean lengths of Woodley and Mercer Kellis et al. [41, 42] Van der hamstring muscles (cm) [41, 42, [86] Made et al. 82, 86] [82]

Number of specimens 6 8 56 Biceps femoris (long head) 43.8 38.93 ± 4.03 42.0 ± 3.4 Biceps femoris (short head) 29.1 28.53 ± 1.92 29.8 ± 3.9 Semitendinosus 43.8 47.03 ± 2.99 44.3 ± 3.9 Semimembranosus 43.8 40.43 ± 2.52 38.7 ± 3.5

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Fig. 11 Lateral view on the innervation of the proximal hamstrings. (1) Ischial tuberosity; (2) sciatic nerve; (3) motor branches of sciatic nerve to long head of the biceps femoris muscle; (4) recurrent branch to the proximal attachment of conjoined tendon rotation of the tibia [75]. These muscles are antagonists of the external rotation generated by the BF [56, 75, 77]. The understanding of their role in the prevention of the valgus collapse, which is the primary mechanism of noncontact ACL injuries [67], is under investigation [90]. The antagonism between the ST and lhBF becomes apparent during a cadaver dissection. The application of a proximally oriented traction force on the ST and lhBF nicely demonstrate their respective functions as internal and exter- nal rotators of the tibia. Interestingly, pulling the SM proxi- mally does not significantly affect internal rotation, which illustrates the muscle’s static function in internal rotation of the tibia through preventing external rotation [LINK to the movie]. The mechanical resistance of junctions in hamstrings seems to be lower than the structure of the actual tendon or muscle tissue. In the present investigation, an appar- ently thinner structure was noticed at two precise areas in the hamstring muscle complex: the conjoined tendon of the lhBF and ST and the conjunction between the lhBF and shBF(Figs. 14, 15a, b, 16). Fig. 12 a–c Lateral view on the innervation of the hamstring muscle complex. (1) Ischial tuberosity; (2) sciatic nerve; (3) motor branch to the long head of the biceps femoris muscle; (4) recurrent branch to the proximal attachment of conjoined tendon; (5) motor branch to the Discussion semitendinosus muscle; (6) motor branch to the semimembranosus muscle; (7) motor branch to the short head of the biceps femoris mus- Most of the studies analysing hamstrings’ anatomical cle structure have shown little variability with respect to the musculotendinous pattern as well as the anatomy of their injury classification systems of which several are new and innervation. Nevertheless, information about the distribu- still under investigation [18, 59, 62, 79]. tion of hamstring injuries is very heterogeneous [6–8, 16, There seems to be a predominance of injuries to the lhBF 20, 21, 23, 28, 30, 39, 45, 63, 72, 84]. This discrepancy may and SM over the ST [6, 8, 20, 21, 23, 39, 45, 72]. It has be explained both by the complexity of their musculoten- been postulated that this may be related to the presence of dinous structure and the heterogeneity of existing muscle overlapping tendons in the lhBF and SM. Some authors

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be associated with high reinjury rate [85] and needs further investigation. The anatomic dissections revealed a recurrent branch of the motor branch of the lhBF. It is located in the area of the proximal conjoined tendon and may be dam- aged in case of an injury [54]. Theoretically, it could also be affected if an inflammatory process of the bursa occurs in this area. The damage of this branch may be responsible for symptoms of the muscle denervation after proximal tendon avulsion, which may remain even after surgical reconstruc- tion. This observation offers a new perspective on the proxi- mal hamstring injuries, but it needs to be further analysed. The anatomical observations highlighted an individual- ised function of each hamstring muscle. There are pointed selective features of the medial hamstring muscles respon- sible for internal tibia rotation versus the lateral hamstring muscles responsible for external tibia rotation [13, 69, 89, 90]. Hamstring muscles have an essential role in the control of tibiofemoral rotation and consequently on the rotational stability of the knee, which has been illustrated by the pre- sent investigation. Although our test was not standardised, it Fig. 13 a, b Entry points of motor branches to the hamstring muscles. may provide an opening for further investigation. (1) Motor branch to the long head of the biceps femoris muscle; (2) The ST tendon is one of the most frequently used auto- two motor branches to the semitendinosus muscle; (3) motor branch to the semimembranosus muscle grafts in orthopaedic surgery. Harvesting this tendon nega- tively impacts its biomechanical function of an active inter- nal rotator, which allows it to prevent the external rotation hypothesised that the raphe in the ST has a protective prop- of the tibia and reduces ST tendon’s direct antagonistic role erty [49, 82]. to the lhBF. Likewise, this may have a consequence on the Morphologically, most injuries appear at the musculo- function and stability of the knee. A recent cadaveric study tendinous junction [21, 30]. The conjoined tendon of the has indeed identified an increased valgus and external rota- lhBF and ST has a very delicate structure located where a tion of the knee after harvesting the ST and gracilis tendons relatively high prevalence of injuries can be observed [7, 16, [48]. Furthermore, while the hamstring tendons have a high 20]. Second, the conjunction between the lhBF and shBF, capacity for regeneration [73], the remaining functional defi- located in the distal part of the hamstring, has also a similar, cits—decreased knee flexion, extension and internal rota- delicate structure. The prevalence of injuries in this area tion, have been reported [44, 74]. A long-term effect of these seems to be reported less frequently [53]. disorders is yet to be established [1]. Hamstring muscle injuries can involve the disruption of The use of hamstrings as graft material renders the matter innervation by damaging motor nerve branches. The nerve of their internal structure a very important one. Recently, the conduction velocity in injured hamstrings is significantly relationships between tendon and muscle inside the mus- lower than in uninjured muscles [47]. This occurrence may cle belly were presented for sartorius, gracilis and peroneus

Table 2 The placement of motor branch entries to hamstring muscles established by measuring a distance from the ischial tuberosity [5, 64, 65, 86]

Rab et al. [64] Woodley and Mercer [86] An et al. [5] Rha et al. [65] a

Number of specimens 30 6 50 32 lhBF 15.1 ± 3.4 cm − 2.8 to − 4 cm (proximally) 14.1 ± 3.3 cm 41.5 ± 9.4% 40–50% One specimen 3.6 cm shBF No information 20 cm 19.1 ± 2.3 cm 56.2 ± 6.0% 70–85% Primary ST 4.75 ± 1.4 cm 4.2–12 cm 7.0 ± 2,2 cm 20.3 ± 5.7% 20–40% Secondary ST 14.47 ± 2.6 cm 7.5–19 cm 20.3 ± 2.9 cm 59.9 ± 6.6% 60–75% SM No information 14.6–21.2 cm 21.1 ± 3.3 cm 62.2 ± 9.2% 60–80% a In the original scale the authors used 0% for the line crossing the medial and lateral tibial condyles and 100% for the ischial tuberosity. For this table, the scale was reversed

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Fig. 14 Location of potential areas of the decreased resist- ance in the hamstring muscle tendon. (1) Conjoined tendon of the semitendinosus and the long head of the biceps femoris; (2) common distal tendon of the long and short head of the biceps femoris

Fig. 16 Lateral view of the thigh with marked areas of potentially decreased resistance of distal biceps femoris tendon (arrowheads). (1) Long head of the biceps femoris muscle; (2) short head of the biceps femoris; (3) quadriceps muscle; (4) patella; (5) intermuscular septum

etc. Detailed photographs can be a very useful instrument longus [15, 26, 27]. Such a relationship in case of hamstrings during preparation for surgical and non-surgical treatment is under the investigation by our group. of hamstring injuries. The direct connection between the hamstring muscle complex and the pelvis through the STL is yet another find- ing worth further research, since the proper tension of ham- Conclusion string muscles is required to achieve the proper position of the pelvis and consequently of the sacrolumbar part of the spine [83]. Knowledge of the anatomy of the hamstrings—their mor- All discussed issues are relevant in daily practice of ortho- phology, innervation, and function, provides valuable insight paedic surgeons, sports medicine specialist, physiotherapists, concerning clinical implications. It helps to improve the

Fig. 15 Posterior view on the proximal posterior thigh with marked potential area of the decreased resistance of conjoined tendon (arrows). (1) Sacrotuberous ligament; (2) ischial tuberosity; (3) gemellus superior, obturator internus, gemellus inferior muscles; (4) sciatic nerve; (5) piriformis muscle; (6) conjoined tendon of the semitendinosus and the long head of the biceps femoris

1 3 Knee Surgery, Sports Traumatology, Arthroscopy understanding of their frequent involvement in pathologic 10. Battermann N, Appell HJ et al (2011) An anatomical study of conditions, and the significant amount of sports-related mus- the proximal hamstring muscle complex to elucidate muscle strains in this region. Int J Sports Med 32(3):211–215 cle injuries and reinjuries. 11. Bejui J, Walch G, Gonon GP et al (1984) Anatomical and func- tional study on the musculus semimembranosus. Anat Clin Acknowledgements We thank Maciej Śmiarowski (https​://www.artla​ 6(3):215–223 borat​ory.eu) who provided photographic documentation. Dr. Robert 12. Bierry G, Simeone FJ, Borg-Stein JP et al (2014) Sacrotuberous Śmigielski wishes to dedicate the article to his mentor—Dr. Bernhard ligament: relationship to normal, torn, and retracted hamstring Segesser. The project was co-funded by the Luxembourg Institute of tendons on MR images. 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