The role of the ligamentum teres in the adult hip: redundant or relevant? A review

The role of the ligamentum teres in the adult hip: redundant or relevant? A review Journal of Hip Preservation Surgery Vol. 5, No. 1, pp. 15–22 doi: 10.1093/jhps/hnx046 Advance Access Publication 10 January 2018 Review article The role of the ligamentum teres in the adult hip: redundant or relevant? A review 1 2 1 John M. O’Donnell *, Brian M. Devitt and Manit Arora Hip Arthroscopy Australia, 21 Erin Street, Richmond, VIC 3121, Australia and Orthosport Victoria, 89 Bridge Road, Richmond, VIC 3121, Australia *Correspondence to: J. M. O’Donnell. E-mail: john@johnodonnell.com.au Submitted 11 March 2017; Revised 21 August 2017; revised version accepted 12 December 2017 ABSTRACT The ligamentum teres (LT) has traditionally been described as a redundant structure with no contribution to hip biomechanics or function. There has been renewed interest in the LT as a source of hip pathology due to the high prevalence of LT pathology observed at the time of hip arthroscopy. The LT acts a secondary stabilizer to supplement the work of the capsular ligaments and works in a sling-like manner to prevent subluxation of the hip at the extremes of motion. The presence of free nerve endings within the LT indicates a definite role in pain gen- eration, with the LT undergoing various mechanical and histological adaptations to hip pathology. given to its role as a hip stabilizer and a pain generator, in INTRODUCTION addition to other proposed roles such as proprioception, The ligamentum teres (LT) and its role in hip function has and synovial fluid distribution. In doing so, the authors been of constant debate since Professor W.S. Savory first present an analysis of the anatomy, the histological struc- presented a paper to the Cambridge Philosophical Society ture, and the biomechanical function of the LT, and the in April 1874 on its function [1]. It has been established various changes the LT undergoes in hip pathology. that the LT assumes an important role in the neonatal hip as a stabilizing structure and a conduit for the blood supply Hip stabilization of the femoral head [2, 3]. However, traditional orthopedic Our current understanding is that the LT acts as a secon- teaching has been to regard the LT as a redundant or ves- dary stabilizer of the hip, supplementing the role of the tigial structure in the adult hip [4]. With the advent of hip capsular ligaments, and works in a sling-like manner to pre- arthroscopy in the last few decades there has been renewed vent subluxation of the femoral head at the extremes of interest in the role the LT plays in hip stability and as a motion. To better understand the role of the LT in hip generator of hip pain [5]. motion, a number of cadaveric studies [11–14] have been The recognition of LT pathology (including synovitis, par- performed in the last decade, including the ‘string model’ tial and complete tears) at the time of hip arthroscopy is studies of Martin et al.[12, 13, 15]. This has been aided by increasingly common with a reported prevalence up to a better understanding of anatomy and histology. 51% [5–7]. Lesions involving the LT have been said to be In open hip preservation surgery, the LT is routinely the third most common cause of hip pain in athletes transected to facilitate delivery of the femoral head. It has undergoing diagnostic arthroscopic procedures [8]. Since the last published reviews of the LT [9, 10], there been shown that resection of the LT leads to long-term mild symptoms of instability (giving way of the hip) in has been a number of new publications regarding the LT. Our aim has been to gather together this new information almost a quarter of patients, despite other pathologies in an update review. The purpose of this review is to define (cam lesions, pincer lesions, labral tears etc.) being the functional role the LT plays in the adult hip with sup- addressed at the time of surgery [16]. This suggests that portive evidence from the literature. Specific focus was the LT has a definite role in stabilization of the hip, a role V C The Author(s) 2018. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by- nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/jhps/article-abstract/5/1/15/4797554 by Ed 'DeepDyve' Gillespie user on 16 March 2018 16  J. M. O’Donnell et al. which may be amplified when there is abnormal bone mor- synovium of the pulvinar and LT are confluent, and both phology, as occurs in femoroacetabular impingement may be impinged during abnormal rotation of the femoral (FAI) or hip dysplasia, or when the other stabilizing struc- head. More recently, the LT has been shown to have multi- tures, such as the capsule, are deficient, as occurs in capsu- ple attachment sites (up to six) from the base of the coty- lar laxity or joint hypermobility. loid fossa [26]. These anatomic findings alone would suggest the LT plays an integral role in the coaptation of Structural anatomy the acetabulum and femoral head in a dynamic manner. Wenger et al.[17] have previously likened the LT to the anterior cruciate ligament (ACL) of the knee. They pro- Mechanical properties posed that the structural anatomy (double bundle) and A key question regarding the importance of the LT, and its ultimate load to failure were similar to the ACL and, as possible similarity to the ACL, relates to its strength and such, the LT may play a role in the hip similar to that of conflicting evidence exists in the literature on this matter. In 2007, Wegner et al. published a frequently cited study in the ACL in the knee. Although it remains unclear whether the LT assumes which they determined the ultimate load to failure of the LT was similar to that of the human ACL. The authors, in the same important role in stability of the hip, there are striking anatomical similarities between the two. The LT is fact, used a porcine model loading the porcine LTs in cus- tom fixation rings and found that the mean ultimate load a pyramidal structure (Fig. 1) with a mean length of 30– 35 mm [11], similar to the ACL. The ligament has a broad to failure of the LT was 882 N, which is similar to a human origin from almost the entire transverse acetabular liga- ACL [17]. More recently, Philippon et al.[27] studied the ment and is attached to the ischial and pubic bases by two human LT, using a custom ball and socket fixture and bands or bundles [18, 19], with the posterior bundle stron- dynamic tensile testing machine, and found a mean ulti- ger than the anterior bundle. Again, this is similar to the mate failure load of 204 N, with a mean native length of ACL [20]. On the ischial side, the origin of the LT is 32 mm and cross-sectional area of 59 mm , with mean described as being stronger and marginally broader, length of 38 mm at its yield point and 53 mm at its failure extending past the osseous cavity of the acetabulum and point [27]. Furthermore, the LT has a linear stiffness of onto the periosteum of the ischium and the capsule [21]. 16 N/mm and elastic modulus of 9.24 MPa, which is signif- Both the LT and the ACL are surrounded by synovium icantly less than a human ACL refuting earlier suggestions [22], which is commonly found to be inflamed at the time of the LT assuming a role similar to the ACL in the knee. of arthroscopy [23]. However, a limitation here is that cadaveric specimens An important anatomic difference between the two liga- with a mean age of 54 years were used, which may not ments is the base from which they originate. While the reflect the true ultimate load to failure in young adults. In ACL arises distinctly from the tibial plateau [20], the LT fact, the ultimate load to failure of the cadaveric LTs is has an attachment on the adjacent postero-inferior aspect more similar to human medial patellofemoral ligament of the acetabular cotyloid fossa which contains fibro-fatty (MPFL) of the knee [28] and the anterolateral ligament of tissue (pulvinar) and small vessels encased in synovium the knee [29], rather than the ACL. [24]. This ‘pulvinar’ is sometimes found to be hyperemic HISTOLOGY in the setting of LT synovitis [25], suggesting the Histologically, the LT is composed of parallel undulating collagen fiber bundles of type I, III, IV and V collagen, along with fibrous and adipose tissue interspersed with blood vessels and nerves [30]. This connective tissue (CT) matrix is surrounded by a layer of investing syno- vium composed of a single layer of cuboidal cells. This his- tological structure is similar to the ACL [31], which has a majority composition of type I collagen fibers arranged in parallel undulating bundles. However, it bears similarity to the MPFL in histology also [32], with loose collagen struc- tures interspersed in a dense collagen framework. Thus, while the LT shares many histological and ana- tomical similarities to the ACL, its mechanical properties Fig. 1. Intra-operative image of the normal LT showing the dou- ble bundle anatomy. are more similar to the MPFL. Downloaded from https://academic.oup.com/jhps/article-abstract/5/1/15/4797554 by Ed 'DeepDyve' Gillespie user on 16 March 2018 The role of the ligamentum teres in the adult hip  17 Biomechanical studies of the LT in isolation The above findings also appear to be consistent with In studies where only the LT, femoral head and acetabu- that same group’s previously devised LT test [37]—pain at lum are preserved [11–13], and the hip is stressed until the the extremes of ER/IR in a position of mid flexion and end point of the LT is reached, it has been found that the slight abduction. We believe this test reproduces the end- range of motion values required to reach such an end- point of the LT at the extreme of the assessed multi-planar point in simple uni-planar motion are well outside the nor- motion, with an inflamed, and/or torn LT inciting a pain mal physiological range of motion of the hip—bone to response within the hip. bone contact occurs well before the end point of the LT is reached in uni-planar motion. This suggests the LT is not Dysplasia of the hip a primary restraint but rather a secondary checkrein. Its As the LT has been proposed to be a secondary stabilizer, main role appears to be in multi-planar motion, or more its role in hip dysplasia is of particular interest, both in natural physiologic motion of the hip, where its end point developmental dysplasia of the hip (DDH) and FAI. It is is reached much earlier, especially in flexion and abduction perhaps the loss of osseous stability, which increases the (similar to a squat position) [13]. importance of the LT as a stabilizer and hence leads to syn- The LT moves with the femoral head, much like a sling, ovitis and/or tears of the LT. and wraps around it in such a way to prevent inferior sub- In the setting of DDH it has been shown that the LT luxation with abduction, posterior subluxation with IR and undergoes various adaptations including: disruption of the anterior subluxation with ER [12]. The LT becomes taut collagen framework; elastic fibers become thicker and with ER and lax with IR in flexion [33]. The LT has main more numerous; cells are irregularly distributed and are in effect on limiting rotations in the mid-high flexion position different stages of functional activity [38]. Further fibro- [15]. It is perhaps in these positions (such as standing to cartilaginous metaplasia is seen within the LT which may sitting, getting into and out of car etc.) where the LT is be secondary to the increased mechanical stress. stressed the most. All the aforementioned studies assume a Interestingly, there appears to be a change in the collagen normal non-dysplastic hip. In the setting of hip dysplasia compositions of the LT in DDH, with an increase in both or capsular laxity, the role of the LT becomes more pro- type III collagen [39] and the ratio of type III to type I col- nounced in stabilizing the hip [34]. lagen [40]. These changes suggest that the LT adapts to increased mechanical stress in DDH by becoming thicker Biomechanical studies of the LT and capsular ligaments and more elastic. This may lead to an increased propensity When the femoral head, acetabulum, LT and the capsular to tear. Interestingly, patients with CT disorders (such as ligaments (iliofemoral, pubofemoral and ischiofemoral) are Marfans and Ehlers-Danlos syndrome) often have muta- preserved in a cadaveric model the contributions of the LT tions to the genes encoding type III collagen [41], it may to hip stability change. van Arkel et al. found that the cap- be that the upregulation of this particular type of collagen, sular ligaments provide the primary restraint to IR and ER as is also the case with DDH patients [39, 40], is partly throughout the complete range of motion of the hip. They responsible for changes to the LT in such patients, in addi- found that the LT has a more defined role a secondary tion to the capsular laxity. restraint in ER during high flexion (>60 ) with neutral/ full adduction [14], with a minimal contribution in IR and FEMOROACETABULAR IMPINGEMENT ER FLEX AB. Further they found that the main restraint In the setting of FAI, tear prevalence of up to 51% has to the high flex ER position is the lateral iliofemoral liga- been reported at the time of hip arthroscopy [5–7]. In ath- ment, advocating for capsular suturing at the time of LT letes with FAI these numbers are higher with a 70% tear debridement/repair. rate (60% partial and 10% complete) which is postulated If the LT assumes a secondary stabilizing role in the occur as a result of increased stress on the LT [42]. The presence of intact capsular ligaments, it may be of more precise reason for the increased prevalence of LT tears in importance when these ligaments are released or lax. This this cohort of patients has yet to be fully elucidated. As in suggestion is supported by the work of O’Donnell et al., the setting of DDH, studies have demonstrated that LT who found that routine anterior capsular tightening, using tears are associated with abnormal bone morphology and either RF or suture plication, leads to significant improve- increased age, with LT tears being more common in ment in results for patients having partial LT tear debride- patients with a low lateral coverage index (center edge ments [35]. This method has resulted in a lesser re-tear rate than their earlier method of LT debridement alone angle—acetabular inclination) [43] and with a lower cen- [36]. ter edge angle alone [44]. This may be due to the levering Downloaded from https://academic.oup.com/jhps/article-abstract/5/1/15/4797554 by Ed 'DeepDyve' Gillespie user on 16 March 2018 18  J. M. O’Donnell et al. effect of the femoral head on the acetabulum causing laxity [49], may be a result of increased laxity of the cap- increased strain in the LT with ultimate failure. sule and subsequent damage to the LT, which in turn leads The presence of LT pathology in the setting of FAI to microinstability of the hip and chondral damage. The often heralds more significant chondral damage to both high prevalence of FAI in athletes [52, 53] compounds this the femoral and acetabular articular surfaces. There is a 3.1 situation by putting the LT at a levering disadvantage. In times higher incidence of chondral damage, particularly to patients with LT tears who have generalized hypermobility, the middle-inferior part of the acetabular fossa and the reconstruction of the LT has improved patient related out- apex of the femoral head, with the presence of LT tears come measures [54, 55]. [44, 45]. Unfortunately, the exact etiology of this associa- tion and whether it is more prevalent in cam or pincer Role in pain generation impingement has not been borne out in these studies. The Degenerative arthritis of the hip is a painful condition. It is question still remains, which comes first the LT tear or the proposed that free nerve endings found in the LT [30, 56] chondral damage? mediate a component of the pain response in degenerative It is possible that the altered biomechanics created in arthritis. Further, it is well established that tears or synovi- the setting of FAI subjects the LT to increased damage. It tis of the LT alone, without the presence of any other hip is known that patients with cam impingement typically pathology, are capable of causing hip pain [8, 10]. have reduced internal rotation [46] which may result in Debridement and/or reconstruction of the ligament alone tightening of the LT. Many of these patients compensate has been shown to be effective in alleviating pain in the by externally rotating their hips during hip flexion to majority of patients [23, 54, 55, 57, 58]. This suggests that account for the cam deformity. It is possible that this the LT is in itself a pain generator, mediated by the free maneuver when performed rapidly, as occurs in sporting nerve endings within the ligament. Radiofrequency abla- activity, may predispose a tight and less compliant LT to tion and or debridement possibly denudes these free nerve excess forces resulting in tearing over time. Further, a defi- endings, eliminating the source of the painful hip, however, cient LT renders the hip less stable particularly during the this has not been proven histologically yet. extremes of motion, as outlined above, which may increase Histology of free nerve endings the shear forces on the articular surfaces of both the femo- ral head and the acetabulum, resulting in accelerated chon- The presence or absence of nerve fibers within the LT has been controversial however more recent studies [30, 59, 60] dral damage. have definitively shown that most, if not all, LT have nerve Benign joint hypermobility fibers, with a mean diameter of 56.5 lm[30], consistent Of particular interest recently has been the pathological with pain mediating unmyelinated fibers. These free nerve changes to the LT in states of capsular laxity and general- endings are concentrated in the center of the ligament [56] ized hypermobility. When the capsular ligaments are lax, as and appear to be of type Iva (nociceptive) variety [56, 60], occurs in generalized hypermobility, the hip has an proving a definite role for the LT as source of pain within increased range of motion, which increases the excursion the hip. Although concentrated in the center of the liga- and endpoints of the LT and possibly leads to its stretching ment, they are sparsely dispersed in the rest of the ligament and eventual tearing. proper. Thus, any tears or synovitis of the LT, mediate pain Patients with generalized hypermobility (as defined by a by exciting these free nerve endings. Beighton test score of 4 or more) have a reduced capsular thickness (capsular laxity) and a high prevalence of partial Degenerative arthritis of the hip tears of the LT [47]. Further, a thin hip capsule alone is In degenerative arthritis of the hip, it has been postulated associated with a higher incidence of LT pathology [48]. that the LT assumes a role more consistent with pain-gen- Athletes are more hypermobile than the general popula- eration [8, 58, 61]. In their study of eleven cadaveric hip tion, with a high incidence of capsular laxity seen in some joints with degeneration, Samptachalit et al. found that the sports in particular such as golf, running, gymnastics [49]. LT shows a spectrum of degenerative changes similar to It is perhaps in this group of athletes where LT damage tendon pathology. The thinnest LT undergoes near com- assumes more significance as a contributor to microinst- plete disruption of the ligament, intermediate thickness ability [50]. The incidence of chondral damage is high LTs show fatty replacement with and without fibromatous across all sports including golf, dancing, soccer and tennis degeneration, fibromatous degeneration with and without [49]. It is proposed that the pattern of chondral damage mucoid degeneration and eosinophilic change, whereas the [51] well described in the setting of athletes with capsular thickest LT show mucoid and fibromatous degeneration Downloaded from https://academic.oup.com/jhps/article-abstract/5/1/15/4797554 by Ed 'DeepDyve' Gillespie user on 16 March 2018 The role of the ligamentum teres in the adult hip  19 with microscopic tears [62]. Dehao et al.[30] further upregulation of free nerve endings in both the capsule and the LT [64]. found occasional foci of osteochondroid and chondroid changes within the CT component which were more prev- Interestingly, recent work on the LT has found small arterioles within the ligament proper which provide a alent with more severe degeneration of the hip. blood supply to the ligament. There are numerous small It is possible that in the degenerative hip, in addition to blood vessels within the CT matrix of the ligament with a well established foci of pain such as the chondral damage, mean diameter of 182 lm. Most of the smaller arteries are the structural damage to the LT alone (Fig. 2) is capable surrounded by a layer of encircling fat [30]. This may pro- of exciting free nerve endings in the ligament. This damage vide a cushioning effect to maintain patency of the vessels appears to be graded, with mild changes in less affected during hip motion and so preserve an unhindered blood hips and more severe metaplastic changes to the LT in supply to the LT. more affected hips. A causal relationship between the It is possible that this unhindered cushioned blood sup- severity of hip arthritis and increasing damage to the LT is ply is what allows the LT to degenerate in a spectrum-like yet to be established by radio-histological studies. manner and also allows nourishment of the LT’s free nerve Shinohara et al.[63] examined the histological changes endings despite the presence of bone to bone contact in in complete LT detachments from the femoral head and severe degenerative arthritis. found that the transition zone of the femoral head attach- ment undergoes histological change including loss of type Role in proprioception II collagen and aggrecan, and abundance of single-stranded The LT was previously thought to serve a proprioceptive DNA positive chondrocytes. The upregulation of single role in the hip, however, the presence or absence of mecha- stranded cells suggests that single stranded DNA damage noreceptors within the LT continues to be a subject of is amplified in the presence of detachment, indicating that debate. There are four types of nerve endings based on detachment or tears are not a purely mechanical event but Freeman and Wyke’s classification [65]: Type I (Ruffini) rather may result from underlying weakening of the transi- low-threshold and slow-adapting; Type II (Pacini) tion zone. low-threshold and fast-adapting; Type III (Golgi) low- This appears to be consistent with the weakening of the threshold and slow-adapting; and type IV (Free nerve end- ligament seen in degenerative arthritis. A weakened liga- ings) high-threshold nociceptors. ment will conduct more stress and hence excite more pain Some recent histological studies [66, 67] have shown fibers. Studying if the concentration of free nerve endings that there is a lack of any of the Type I-III mechanorecep- in the degenerating LT increase or decrease will help us tors in either the LT or the hip joint capsule. However, better understand the contribution of the LT as a pain gen- Moraes et al.[64] found all four types of mechanorecep- erator in the degenerating hip. To this effect, a recent study tors in the labrum, capsule and the LT, and an upregula- has found that in the setting of arthritis, there is a definite tion of these receptors in the setting of arthrosis. It is possible that the suggested proprioceptive role of the LT is mediated by the presence of mechanoreceptors, however, the free nerve endings themselves may subserve a proprioceptive role in the painful hip. Role in synovial fluid distribution Under normal physiologic loads, the hip joint is lubricated by fluid film lubrication [68]. The LT, by virtue of its intra- articular position and its motion with femoral head rota- tion, has proposed to have a ‘windshield wiper’ effect to facilitate synovial fluid distribution [4]. It is possible that as the femoral head rotates, the LT acting in a sling-like man- ner, distributes synovial fluid across the femoral head sur- face, much the same way as a windshield wiper of the car. This may allow for more equal distribution of synovial fluid across the hip joint, however, this has not yet been proven. Although this theory has often been quoted, the original Fig. 2. Intra-operative image of a degenerate LT in the setting of early osteoarthritis of the hip. source of the theory is uncertain. Downloaded from https://academic.oup.com/jhps/article-abstract/5/1/15/4797554 by Ed 'DeepDyve' Gillespie user on 16 March 2018 20  J. M. O’Donnell et al. 9. Bardakos NV, Villar RN. The ligamentum teres of the adult hip. 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Arthritis Res Ther muscles. Br J Surg 1967; 54: 990–1001. 2017; 19: 18. 66. Muratli HH, Bic¸imoglu A, Tabak YA et al. Mechanoreceptor eval- 70. Scanzello CR, Goldring SR. The role of synovitis in osteoarthritis uation of hip joint capsule and ligamentum capitis femoris in pathogenesis. Bone 2012; 51: 249–57. Downloaded from https://academic.oup.com/jhps/article-abstract/5/1/15/4797554 by Ed 'DeepDyve' Gillespie user on 16 March 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Hip Preservation Surgery Oxford University Press

The role of the ligamentum teres in the adult hip: redundant or relevant? A review

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Journal of Hip Preservation Surgery Vol. 5, No. 1, pp. 15–22 doi: 10.1093/jhps/hnx046 Advance Access Publication 10 January 2018 Review article The role of the ligamentum teres in the adult hip: redundant or relevant? A review 1 2 1 John M. O’Donnell *, Brian M. Devitt and Manit Arora Hip Arthroscopy Australia, 21 Erin Street, Richmond, VIC 3121, Australia and Orthosport Victoria, 89 Bridge Road, Richmond, VIC 3121, Australia *Correspondence to: J. M. O’Donnell. E-mail: john@johnodonnell.com.au Submitted 11 March 2017; Revised 21 August 2017; revised version accepted 12 December 2017 ABSTRACT The ligamentum teres (LT) has traditionally been described as a redundant structure with no contribution to hip biomechanics or function. There has been renewed interest in the LT as a source of hip pathology due to the high prevalence of LT pathology observed at the time of hip arthroscopy. The LT acts a secondary stabilizer to supplement the work of the capsular ligaments and works in a sling-like manner to prevent subluxation of the hip at the extremes of motion. The presence of free nerve endings within the LT indicates a definite role in pain gen- eration, with the LT undergoing various mechanical and histological adaptations to hip pathology. given to its role as a hip stabilizer and a pain generator, in INTRODUCTION addition to other proposed roles such as proprioception, The ligamentum teres (LT) and its role in hip function has and synovial fluid distribution. In doing so, the authors been of constant debate since Professor W.S. Savory first present an analysis of the anatomy, the histological struc- presented a paper to the Cambridge Philosophical Society ture, and the biomechanical function of the LT, and the in April 1874 on its function [1]. It has been established various changes the LT undergoes in hip pathology. that the LT assumes an important role in the neonatal hip as a stabilizing structure and a conduit for the blood supply Hip stabilization of the femoral head [2, 3]. However, traditional orthopedic Our current understanding is that the LT acts as a secon- teaching has been to regard the LT as a redundant or ves- dary stabilizer of the hip, supplementing the role of the tigial structure in the adult hip [4]. With the advent of hip capsular ligaments, and works in a sling-like manner to pre- arthroscopy in the last few decades there has been renewed vent subluxation of the femoral head at the extremes of interest in the role the LT plays in hip stability and as a motion. To better understand the role of the LT in hip generator of hip pain [5]. motion, a number of cadaveric studies [11–14] have been The recognition of LT pathology (including synovitis, par- performed in the last decade, including the ‘string model’ tial and complete tears) at the time of hip arthroscopy is studies of Martin et al.[12, 13, 15]. This has been aided by increasingly common with a reported prevalence up to a better understanding of anatomy and histology. 51% [5–7]. Lesions involving the LT have been said to be In open hip preservation surgery, the LT is routinely the third most common cause of hip pain in athletes transected to facilitate delivery of the femoral head. It has undergoing diagnostic arthroscopic procedures [8]. Since the last published reviews of the LT [9, 10], there been shown that resection of the LT leads to long-term mild symptoms of instability (giving way of the hip) in has been a number of new publications regarding the LT. Our aim has been to gather together this new information almost a quarter of patients, despite other pathologies in an update review. The purpose of this review is to define (cam lesions, pincer lesions, labral tears etc.) being the functional role the LT plays in the adult hip with sup- addressed at the time of surgery [16]. This suggests that portive evidence from the literature. Specific focus was the LT has a definite role in stabilization of the hip, a role V C The Author(s) 2018. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by- nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/jhps/article-abstract/5/1/15/4797554 by Ed 'DeepDyve' Gillespie user on 16 March 2018 16  J. M. O’Donnell et al. which may be amplified when there is abnormal bone mor- synovium of the pulvinar and LT are confluent, and both phology, as occurs in femoroacetabular impingement may be impinged during abnormal rotation of the femoral (FAI) or hip dysplasia, or when the other stabilizing struc- head. More recently, the LT has been shown to have multi- tures, such as the capsule, are deficient, as occurs in capsu- ple attachment sites (up to six) from the base of the coty- lar laxity or joint hypermobility. loid fossa [26]. These anatomic findings alone would suggest the LT plays an integral role in the coaptation of Structural anatomy the acetabulum and femoral head in a dynamic manner. Wenger et al.[17] have previously likened the LT to the anterior cruciate ligament (ACL) of the knee. They pro- Mechanical properties posed that the structural anatomy (double bundle) and A key question regarding the importance of the LT, and its ultimate load to failure were similar to the ACL and, as possible similarity to the ACL, relates to its strength and such, the LT may play a role in the hip similar to that of conflicting evidence exists in the literature on this matter. In 2007, Wegner et al. published a frequently cited study in the ACL in the knee. Although it remains unclear whether the LT assumes which they determined the ultimate load to failure of the LT was similar to that of the human ACL. The authors, in the same important role in stability of the hip, there are striking anatomical similarities between the two. The LT is fact, used a porcine model loading the porcine LTs in cus- tom fixation rings and found that the mean ultimate load a pyramidal structure (Fig. 1) with a mean length of 30– 35 mm [11], similar to the ACL. The ligament has a broad to failure of the LT was 882 N, which is similar to a human origin from almost the entire transverse acetabular liga- ACL [17]. More recently, Philippon et al.[27] studied the ment and is attached to the ischial and pubic bases by two human LT, using a custom ball and socket fixture and bands or bundles [18, 19], with the posterior bundle stron- dynamic tensile testing machine, and found a mean ulti- ger than the anterior bundle. Again, this is similar to the mate failure load of 204 N, with a mean native length of ACL [20]. On the ischial side, the origin of the LT is 32 mm and cross-sectional area of 59 mm , with mean described as being stronger and marginally broader, length of 38 mm at its yield point and 53 mm at its failure extending past the osseous cavity of the acetabulum and point [27]. Furthermore, the LT has a linear stiffness of onto the periosteum of the ischium and the capsule [21]. 16 N/mm and elastic modulus of 9.24 MPa, which is signif- Both the LT and the ACL are surrounded by synovium icantly less than a human ACL refuting earlier suggestions [22], which is commonly found to be inflamed at the time of the LT assuming a role similar to the ACL in the knee. of arthroscopy [23]. However, a limitation here is that cadaveric specimens An important anatomic difference between the two liga- with a mean age of 54 years were used, which may not ments is the base from which they originate. While the reflect the true ultimate load to failure in young adults. In ACL arises distinctly from the tibial plateau [20], the LT fact, the ultimate load to failure of the cadaveric LTs is has an attachment on the adjacent postero-inferior aspect more similar to human medial patellofemoral ligament of the acetabular cotyloid fossa which contains fibro-fatty (MPFL) of the knee [28] and the anterolateral ligament of tissue (pulvinar) and small vessels encased in synovium the knee [29], rather than the ACL. [24]. This ‘pulvinar’ is sometimes found to be hyperemic HISTOLOGY in the setting of LT synovitis [25], suggesting the Histologically, the LT is composed of parallel undulating collagen fiber bundles of type I, III, IV and V collagen, along with fibrous and adipose tissue interspersed with blood vessels and nerves [30]. This connective tissue (CT) matrix is surrounded by a layer of investing syno- vium composed of a single layer of cuboidal cells. This his- tological structure is similar to the ACL [31], which has a majority composition of type I collagen fibers arranged in parallel undulating bundles. However, it bears similarity to the MPFL in histology also [32], with loose collagen struc- tures interspersed in a dense collagen framework. Thus, while the LT shares many histological and ana- tomical similarities to the ACL, its mechanical properties Fig. 1. Intra-operative image of the normal LT showing the dou- ble bundle anatomy. are more similar to the MPFL. Downloaded from https://academic.oup.com/jhps/article-abstract/5/1/15/4797554 by Ed 'DeepDyve' Gillespie user on 16 March 2018 The role of the ligamentum teres in the adult hip  17 Biomechanical studies of the LT in isolation The above findings also appear to be consistent with In studies where only the LT, femoral head and acetabu- that same group’s previously devised LT test [37]—pain at lum are preserved [11–13], and the hip is stressed until the the extremes of ER/IR in a position of mid flexion and end point of the LT is reached, it has been found that the slight abduction. We believe this test reproduces the end- range of motion values required to reach such an end- point of the LT at the extreme of the assessed multi-planar point in simple uni-planar motion are well outside the nor- motion, with an inflamed, and/or torn LT inciting a pain mal physiological range of motion of the hip—bone to response within the hip. bone contact occurs well before the end point of the LT is reached in uni-planar motion. This suggests the LT is not Dysplasia of the hip a primary restraint but rather a secondary checkrein. Its As the LT has been proposed to be a secondary stabilizer, main role appears to be in multi-planar motion, or more its role in hip dysplasia is of particular interest, both in natural physiologic motion of the hip, where its end point developmental dysplasia of the hip (DDH) and FAI. It is is reached much earlier, especially in flexion and abduction perhaps the loss of osseous stability, which increases the (similar to a squat position) [13]. importance of the LT as a stabilizer and hence leads to syn- The LT moves with the femoral head, much like a sling, ovitis and/or tears of the LT. and wraps around it in such a way to prevent inferior sub- In the setting of DDH it has been shown that the LT luxation with abduction, posterior subluxation with IR and undergoes various adaptations including: disruption of the anterior subluxation with ER [12]. The LT becomes taut collagen framework; elastic fibers become thicker and with ER and lax with IR in flexion [33]. The LT has main more numerous; cells are irregularly distributed and are in effect on limiting rotations in the mid-high flexion position different stages of functional activity [38]. Further fibro- [15]. It is perhaps in these positions (such as standing to cartilaginous metaplasia is seen within the LT which may sitting, getting into and out of car etc.) where the LT is be secondary to the increased mechanical stress. stressed the most. All the aforementioned studies assume a Interestingly, there appears to be a change in the collagen normal non-dysplastic hip. In the setting of hip dysplasia compositions of the LT in DDH, with an increase in both or capsular laxity, the role of the LT becomes more pro- type III collagen [39] and the ratio of type III to type I col- nounced in stabilizing the hip [34]. lagen [40]. These changes suggest that the LT adapts to increased mechanical stress in DDH by becoming thicker Biomechanical studies of the LT and capsular ligaments and more elastic. This may lead to an increased propensity When the femoral head, acetabulum, LT and the capsular to tear. Interestingly, patients with CT disorders (such as ligaments (iliofemoral, pubofemoral and ischiofemoral) are Marfans and Ehlers-Danlos syndrome) often have muta- preserved in a cadaveric model the contributions of the LT tions to the genes encoding type III collagen [41], it may to hip stability change. van Arkel et al. found that the cap- be that the upregulation of this particular type of collagen, sular ligaments provide the primary restraint to IR and ER as is also the case with DDH patients [39, 40], is partly throughout the complete range of motion of the hip. They responsible for changes to the LT in such patients, in addi- found that the LT has a more defined role a secondary tion to the capsular laxity. restraint in ER during high flexion (>60 ) with neutral/ full adduction [14], with a minimal contribution in IR and FEMOROACETABULAR IMPINGEMENT ER FLEX AB. Further they found that the main restraint In the setting of FAI, tear prevalence of up to 51% has to the high flex ER position is the lateral iliofemoral liga- been reported at the time of hip arthroscopy [5–7]. In ath- ment, advocating for capsular suturing at the time of LT letes with FAI these numbers are higher with a 70% tear debridement/repair. rate (60% partial and 10% complete) which is postulated If the LT assumes a secondary stabilizing role in the occur as a result of increased stress on the LT [42]. The presence of intact capsular ligaments, it may be of more precise reason for the increased prevalence of LT tears in importance when these ligaments are released or lax. This this cohort of patients has yet to be fully elucidated. As in suggestion is supported by the work of O’Donnell et al., the setting of DDH, studies have demonstrated that LT who found that routine anterior capsular tightening, using tears are associated with abnormal bone morphology and either RF or suture plication, leads to significant improve- increased age, with LT tears being more common in ment in results for patients having partial LT tear debride- patients with a low lateral coverage index (center edge ments [35]. This method has resulted in a lesser re-tear rate than their earlier method of LT debridement alone angle—acetabular inclination) [43] and with a lower cen- [36]. ter edge angle alone [44]. This may be due to the levering Downloaded from https://academic.oup.com/jhps/article-abstract/5/1/15/4797554 by Ed 'DeepDyve' Gillespie user on 16 March 2018 18  J. M. O’Donnell et al. effect of the femoral head on the acetabulum causing laxity [49], may be a result of increased laxity of the cap- increased strain in the LT with ultimate failure. sule and subsequent damage to the LT, which in turn leads The presence of LT pathology in the setting of FAI to microinstability of the hip and chondral damage. The often heralds more significant chondral damage to both high prevalence of FAI in athletes [52, 53] compounds this the femoral and acetabular articular surfaces. There is a 3.1 situation by putting the LT at a levering disadvantage. In times higher incidence of chondral damage, particularly to patients with LT tears who have generalized hypermobility, the middle-inferior part of the acetabular fossa and the reconstruction of the LT has improved patient related out- apex of the femoral head, with the presence of LT tears come measures [54, 55]. [44, 45]. Unfortunately, the exact etiology of this associa- tion and whether it is more prevalent in cam or pincer Role in pain generation impingement has not been borne out in these studies. The Degenerative arthritis of the hip is a painful condition. It is question still remains, which comes first the LT tear or the proposed that free nerve endings found in the LT [30, 56] chondral damage? mediate a component of the pain response in degenerative It is possible that the altered biomechanics created in arthritis. Further, it is well established that tears or synovi- the setting of FAI subjects the LT to increased damage. It tis of the LT alone, without the presence of any other hip is known that patients with cam impingement typically pathology, are capable of causing hip pain [8, 10]. have reduced internal rotation [46] which may result in Debridement and/or reconstruction of the ligament alone tightening of the LT. Many of these patients compensate has been shown to be effective in alleviating pain in the by externally rotating their hips during hip flexion to majority of patients [23, 54, 55, 57, 58]. This suggests that account for the cam deformity. It is possible that this the LT is in itself a pain generator, mediated by the free maneuver when performed rapidly, as occurs in sporting nerve endings within the ligament. Radiofrequency abla- activity, may predispose a tight and less compliant LT to tion and or debridement possibly denudes these free nerve excess forces resulting in tearing over time. Further, a defi- endings, eliminating the source of the painful hip, however, cient LT renders the hip less stable particularly during the this has not been proven histologically yet. extremes of motion, as outlined above, which may increase Histology of free nerve endings the shear forces on the articular surfaces of both the femo- ral head and the acetabulum, resulting in accelerated chon- The presence or absence of nerve fibers within the LT has been controversial however more recent studies [30, 59, 60] dral damage. have definitively shown that most, if not all, LT have nerve Benign joint hypermobility fibers, with a mean diameter of 56.5 lm[30], consistent Of particular interest recently has been the pathological with pain mediating unmyelinated fibers. These free nerve changes to the LT in states of capsular laxity and general- endings are concentrated in the center of the ligament [56] ized hypermobility. When the capsular ligaments are lax, as and appear to be of type Iva (nociceptive) variety [56, 60], occurs in generalized hypermobility, the hip has an proving a definite role for the LT as source of pain within increased range of motion, which increases the excursion the hip. Although concentrated in the center of the liga- and endpoints of the LT and possibly leads to its stretching ment, they are sparsely dispersed in the rest of the ligament and eventual tearing. proper. Thus, any tears or synovitis of the LT, mediate pain Patients with generalized hypermobility (as defined by a by exciting these free nerve endings. Beighton test score of 4 or more) have a reduced capsular thickness (capsular laxity) and a high prevalence of partial Degenerative arthritis of the hip tears of the LT [47]. Further, a thin hip capsule alone is In degenerative arthritis of the hip, it has been postulated associated with a higher incidence of LT pathology [48]. that the LT assumes a role more consistent with pain-gen- Athletes are more hypermobile than the general popula- eration [8, 58, 61]. In their study of eleven cadaveric hip tion, with a high incidence of capsular laxity seen in some joints with degeneration, Samptachalit et al. found that the sports in particular such as golf, running, gymnastics [49]. LT shows a spectrum of degenerative changes similar to It is perhaps in this group of athletes where LT damage tendon pathology. The thinnest LT undergoes near com- assumes more significance as a contributor to microinst- plete disruption of the ligament, intermediate thickness ability [50]. The incidence of chondral damage is high LTs show fatty replacement with and without fibromatous across all sports including golf, dancing, soccer and tennis degeneration, fibromatous degeneration with and without [49]. It is proposed that the pattern of chondral damage mucoid degeneration and eosinophilic change, whereas the [51] well described in the setting of athletes with capsular thickest LT show mucoid and fibromatous degeneration Downloaded from https://academic.oup.com/jhps/article-abstract/5/1/15/4797554 by Ed 'DeepDyve' Gillespie user on 16 March 2018 The role of the ligamentum teres in the adult hip  19 with microscopic tears [62]. Dehao et al.[30] further upregulation of free nerve endings in both the capsule and the LT [64]. found occasional foci of osteochondroid and chondroid changes within the CT component which were more prev- Interestingly, recent work on the LT has found small arterioles within the ligament proper which provide a alent with more severe degeneration of the hip. blood supply to the ligament. There are numerous small It is possible that in the degenerative hip, in addition to blood vessels within the CT matrix of the ligament with a well established foci of pain such as the chondral damage, mean diameter of 182 lm. Most of the smaller arteries are the structural damage to the LT alone (Fig. 2) is capable surrounded by a layer of encircling fat [30]. This may pro- of exciting free nerve endings in the ligament. This damage vide a cushioning effect to maintain patency of the vessels appears to be graded, with mild changes in less affected during hip motion and so preserve an unhindered blood hips and more severe metaplastic changes to the LT in supply to the LT. more affected hips. A causal relationship between the It is possible that this unhindered cushioned blood sup- severity of hip arthritis and increasing damage to the LT is ply is what allows the LT to degenerate in a spectrum-like yet to be established by radio-histological studies. manner and also allows nourishment of the LT’s free nerve Shinohara et al.[63] examined the histological changes endings despite the presence of bone to bone contact in in complete LT detachments from the femoral head and severe degenerative arthritis. found that the transition zone of the femoral head attach- ment undergoes histological change including loss of type Role in proprioception II collagen and aggrecan, and abundance of single-stranded The LT was previously thought to serve a proprioceptive DNA positive chondrocytes. The upregulation of single role in the hip, however, the presence or absence of mecha- stranded cells suggests that single stranded DNA damage noreceptors within the LT continues to be a subject of is amplified in the presence of detachment, indicating that debate. There are four types of nerve endings based on detachment or tears are not a purely mechanical event but Freeman and Wyke’s classification [65]: Type I (Ruffini) rather may result from underlying weakening of the transi- low-threshold and slow-adapting; Type II (Pacini) tion zone. low-threshold and fast-adapting; Type III (Golgi) low- This appears to be consistent with the weakening of the threshold and slow-adapting; and type IV (Free nerve end- ligament seen in degenerative arthritis. A weakened liga- ings) high-threshold nociceptors. ment will conduct more stress and hence excite more pain Some recent histological studies [66, 67] have shown fibers. Studying if the concentration of free nerve endings that there is a lack of any of the Type I-III mechanorecep- in the degenerating LT increase or decrease will help us tors in either the LT or the hip joint capsule. However, better understand the contribution of the LT as a pain gen- Moraes et al.[64] found all four types of mechanorecep- erator in the degenerating hip. To this effect, a recent study tors in the labrum, capsule and the LT, and an upregula- has found that in the setting of arthritis, there is a definite tion of these receptors in the setting of arthrosis. It is possible that the suggested proprioceptive role of the LT is mediated by the presence of mechanoreceptors, however, the free nerve endings themselves may subserve a proprioceptive role in the painful hip. Role in synovial fluid distribution Under normal physiologic loads, the hip joint is lubricated by fluid film lubrication [68]. The LT, by virtue of its intra- articular position and its motion with femoral head rota- tion, has proposed to have a ‘windshield wiper’ effect to facilitate synovial fluid distribution [4]. It is possible that as the femoral head rotates, the LT acting in a sling-like man- ner, distributes synovial fluid across the femoral head sur- face, much the same way as a windshield wiper of the car. This may allow for more equal distribution of synovial fluid across the hip joint, however, this has not yet been proven. Although this theory has often been quoted, the original Fig. 2. Intra-operative image of a degenerate LT in the setting of early osteoarthritis of the hip. source of the theory is uncertain. Downloaded from https://academic.oup.com/jhps/article-abstract/5/1/15/4797554 by Ed 'DeepDyve' Gillespie user on 16 March 2018 20  J. M. O’Donnell et al. 9. Bardakos NV, Villar RN. The ligamentum teres of the adult hip. Synovitis is being increasingly recognized as central to J Bone Joint Surg Br 2009; 91: 8–15. degenerative arthritis of the hip [69, 70]. It is possible that 10. O’Donnell JM, Pritchard M, Salas AP et al. The ligamentum in degenerative arthritis of the hip, due to the increased teres—its increasing importance. J Hip Preserv Surg 2014; 1: 3–11. fluid secondary to synovitis and the thickening and meta- 11. Demange MK, Kakuda CMS, Pereira CAM et al. Influence of the plasia of the LT as previously discussed, the LT is both femoral head ligament on hip mechanical function. Acta Ortope´dica Bras 2007; 15: 187–90. weaker and at a mechanical disadvantage to distribute the 12. Martin RL, Kivlan BR, Clemente FR. A cadaveric model for liga- increased volume of synovial fluid within the early degener- mentum teres function: a pilot study. Knee Surg Sports Traumatol ate hip. This may affect the proper lubrication of the hip, Arthrosc 2013; 21: 1689–93. and accelerate damage to the hip cartilage. 13. Kivlan BR, Richard Clemente F, Martin RL et al. Function of the ligamentum teres during multi-planar movement of the hip joint. CONCLUSION Knee Surg Sports Traumatol Arthrosc 2013; 21: 1664–8. The LT is not a redundant structure in the adult hip. Its 14. van Arkel RJ, Amis AA, Cobb JP et al. The capsular ligaments pro- vide more hip rotational restraint than the acetabular labrum and primary role appears to be as a secondary stabilizer to sup- the ligamentum teres: an experimental study. Bone Joint J 2015; plement the work of the capsular ligaments, particularly in 97-B: 484–91. mid-flexion, abduction/adduction and rotation. It may 15. Martin HD, Hatem MA, Kivlan BR et al. Function of the ligamen- have a more defined role to prevent subluxation in a sling tum teres in limiting hip rotation: a cadaveric study. Arthroscopy function around the femoral head. It acts as a source of 2014; 30: 1085–91. pain within the hip joint, a role subserved by the free nerve 16. Phillips AR, Bartlett G, Norton M et al. Hip stability after ligamen- tum teres resection during surgical dislocation for cam impinge- endings in the ligament, and undergoes mechanical and ment. Hip Int J Clin Exp Res Hip Pathol Ther 2012; 22: 329–34. histological transformations based on hip pathology. These 17. Wenger D, Miyanji F, Mahar A et al. The mechanical properties same free nerve endings may serve a secondary propriocep- of the ligamentum teres: a pilot study to assess its potential for tive role in the painful hip. Further, the LT may act to dis- improving stability in children’s hip surgery. J Pediatr Orthop tribute synovial fluid within the hip joint. 2007; 27: 408–10. 18. Perumal V, Woodley SJ, Nicholson HD. Ligament of the head of femur: a comprehensive review of its anatomy, embryology, and FUNDING potential function. Clin Anat N Y N 2016; 29: 247–55. 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Journal of Hip Preservation SurgeryOxford University Press

Published: Jan 1, 2018

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