Journal of Orthopaedic Research 19 (2001) 359-364

Journal of Orthopaedic

Research www.elsevier.nl/locate/orthres

Regional material properties of the human hip joint capsule ligaments John Hewitt, Farshid Guilak, Richard Glisson, T. Parker Vail *

Dirision of Orthopaerlii. Surgery, Department of Surgery, Orthopnedic~ Reseurch Luhwatories, Duke (Jnioc~rsity Afetiical Center, Box 3332 Durhum, NC 177710, USA

Received 17 July 2000; accepted 15 September 2000

Abstract

The hip joint capsule functions to constrain translation between the femur and acetabulum while allowing rotational and planar movements. Despite the crucial role it plays in the pathogenesis of hip instability, little is known about its biomechanical properties. The goal of this study was to determine the regional material properties of the iliofemoral and ischiofemoral ligaments of the capsule.

Ten human cadaveric specimens of each ligament were tested to failure in tension. The stress at failure, strain at failure, strain energy density at failure, toe- and linear-region elastic moduli, and the Poisson’s ratio were measured for each ligament.

The strain to failure was greatest in the ischiofemoral ligament, while no significant difference was noted in failure stress by region or ligament. The Young’s moduli of elasticity ranged from 76.1 to 285.8 MPa among the different ligaments, and were generally consistent with properties previously reported for the shoulder capsule. The elastic moduli and strain energy density at failure differed by region. No significant differences in Poisson’s ratio were found by region or ligament. The average Poisson’s ratio was approximately 1.4, consistent with anisotropic behavior of ligamentous tissues.

Understanding the material properties of the hip capsule may help the orthopaedic surgeon better understand normal ligament function, and thereby choose a surgical approach or strategy of repair. Furthermore, knowledge of the normal mechanical function of the hip capsule ligaments could assist in the evaluation of the success of a repair. 0 2001 Orthopaedic Research Society. Published by Elsevier Science Ltd. All rights reserved.

Introduction

The hip joint capsule functions in conjunction with the bony components of the hip joint to constrain translation between the head of the femur and the ace- tabulum while allowing combinations of rotation and planar movemen.ts [I 51. Despite this important biome- chanical function, little is currently known of its intrinsic anatomy and mechanical properties. The relative lack of information is surprising considering that the hip cap- sule is often partially or completely excised during total hip arthroplasty for treatment of arthritis and hemiar- throplasty for displaced intracapsular hip fractures. The presence and proper function of the hip capsule, as well as the surgical approach through the hip capsule are two factors thought to be related to the incidence of hip dislocation after these procedures [ 16,211.

*Corresponding author. Tel.: +1-919-684-6166; fax: +1-919-681- 779s.

E-mail address: vai10001@mc.duke.edu (T. Parker Vail).

The hip capsule is well known for its role in providing a vascular supply to the femoral head in adults [37]. The most important and anatomically consistent of the lig- aments of the capsule are the iliofemoral and ischiofe- moral ligaments. The iliofemoral ligament, known also as the Y-ligament of Bigelow, originates between the anterior inferior iliac spine and the acetabulum and spirals medially to its insertion along the intertrochan- teric line anterior to the hip joint (Fig. 1) [11,15]. It functions to restrict extension of the hip, providing a static restraint with full hip extension which allows erect posture to be maintained without constant muscular action [I 1,151. The ischiofemoral ligament originates from the ischial rim of the acetabulum, follows the spiral of the iliofemoral ligament as it crosses the joint and inserts around the posterior aspect of the femoral neck (Fig. 2) [11,15]. Due to its posterior location, it restricts internal rotation but also adduction when the hip is flexed [I 11.

In the absence of previous surgery, dislocation of the hip o r injury to the hip capsule ligaments generally requires relatively high forces in adults, and less in

0736-0266/01/$ - see front matter 0 2001 Orthopaedic Research Society. Published by Elsevier Science Ltd. All rights reserved. PII: S 0 7 3 6 - 0 2 6 6 ( 0 0 ) 0 0 0 3 5 - 8

360 J. Hrwi t t et al. I Journal of Ortlwpuedic Rescurch 19 (-7001 i 359-364

i Anterior Inferior ' \ \ I

Iliac Spine \ \ ,~ '1 i \\ Inferior

Trochanter i

Fig, 1. Anterior view of the hip joint indicating the anatomy of the hip joint capsule ligaments. The iliofemoral ligaments are shaded gray.

,

Ischial )<IT// Lesser / Trochanter I

Tuberosity i > I

Fig. 2. Posterior view of the hip joint indicating the anatomy of the hip joint capsule ligaments. The ischiofemoral ligament is shaded gray.

children [19,23]. Dislocation of the hip in sports is rare, although subluxation and dislocation have been re- ported to occur in football, rugby, jogging, water skiing, and snow skiing [6,19,20,22,25,29,30]. Interestingly, posterior dislocations occur far more commonly in sports and trauma than anterior dislocations of the hip [7,19,36]. One of the motivating factors in studying the biomechanics of the hip capsule is to better understand the injury patterns and postoperative dislocation pat- terns seen clinically.

While the anatomy of the hip joint capsule has been well described, little or no information is currently available on the material properties of the ligaments comprising the capsule [ll]. The specific aim of this study was to characterize the material properties of the iliofemoral and ischiofemoral ligaments. Constant- strain-rate tests of bone-ligament-bone complexes were

performed in conjunction with digital video analysis to determine the stress-strain relationship of the ligaments and to calculate the toe- and linear-region tangent mo- duli, Poisson's ratio, and failure properties of each lig- ament. Since the shape of these ligaments is not rectangular in the dimensions of length and width, we also compared the material properties between regions within each ligament.

Given the greater incidence of posterior dislocations of the hip compared to anterior dislocations, as well as the greater thickness of the anterior capsule compared to the posterior, one would expect the anterior elements of the capsule to be stronger than the posterior elements. We hypothesized that the iliofemoral ligaments would withstand greater force at failure compared to the is- chiofemoral ligament, but that the stress at failure would not differ significantly. We also predicted that the iliofemoral ligaments would be stiffer than the ischiofe- moral ligament. Knowledge of the properties of these ligaments will provide useful information to clinicians considering injury patterns and surgical approaches to the hip in addition to improving the understanding of ligament mechanics in general.

Methods

Ten specimens of each ligament were obtained from fresh frozen human cadavera (7 females, 3 males, age range: 50-99). The hip joints were removed en bloc by removing all soft tissues except the joint capsule ligaments and surrounding bone [3,24,3 I ] . The ilium was tran- sected immediately proximal to the anterior inferior iliac spine and the posterior inferior iliac spine. The ischium was sectioned through the ischial tuberosity and the pubis through the pubic ramus. The femur was transected immediately distal to the lesser trochanter. Each hip joint was examined under direct visualization for evidence of gross pathology such as fibrillation or erosions on the articular surfaces or marked bone loss. The samples were discarded if gross pathology was noted.

The two ligaments of the hip capsule were identified by their origin. insertion, fiber orientation and thickness according to previously de- scribed anatomical characteristics (Figs. 1 and 2) [ I 1,151. The liga- ments were separated from the remaining joint capsule by sharply dividing the capsule parallel to the fiber orientation along the edge of the ligament [3]. The acetabulum and femur were then sectioned with an oscillating saw around the origin and insertion to create a bone- ligament-bone specimen with bone blocks 2-5 cm in length [2,3]. The iliofemoral ligament was divided in half. parallel to its fiber orienta- tion, creating bone-ligament-bone specimens corresponding to the superior iliofemoral ligament and the inferior iliofemoral ligament as described previously [ll].

The cross-sectional area of each specimen was measured at four equally spaced locations along the ligament using the established area micrometer technique [4,31,33,35]. The micrometer activates a plunger compressing the ligament within a rectangular slot. The displacement measured by the micrometer is multiplied by the known width of the slot to generate the cross-sectional area. Each bone block was then inserted into polyester resin in an aluminum cylinder [2,26]. The specimens were mounted in a uniaxial servohydraulic testing machine (Model 1321, Instron, Canton, MA) with the fiber axis in line with the axis of displacement [2,3,14,24,26]. The fiber axis was determined by directly visualizing the orientation of the ligament fibers. The lower pot was clamped to the machine base, and the upper pot was attached to a load cell (Model 4110571-01, Sensotec, Columbus, OH). The load cell was attached to a universal joint, which was mounted to the actuator piston. The universal joint allowed the ligament fibers to orient with three degrees of freedom [2]. During all manipulations the ligaments

J. Hewitt et al. I Journal of Orthopaedic Research 19 (2001) 359-364 361

were maintained in an unloaded state and kept moist by spraying them with normal saline [2,14,24,26,32].

Each ligament was placed under a tensile tare load of 0.98 N and allowed to equilibrate [2,3,24,26,32-341. For optical measurements of strain, five equally spaced lines were marked transversely on the specimen using Verhoeff‘s stain [4,8,26,31,32,35]. A preconditioning routine of 10 cycles of loading to 5% strain was conducted at a rate of 0.5 mmls [32]. Each ligament was then loaded to failure at a dis- placement rate of 0.04 m d s [2,3,26]. This rate was selected to mini- mize the viscoelastic effects of the material [2].

The tensile force on the ligament was measured from the load cell [32]. Material displacement was measured by a video analysis system similar to previously described methods [24,8,26,32,33,35]. A CCD camera (Model 4915-2000/0000, Cohu, San Diego, CA) was used to record images of the ligament to an S-VHS videotape recorder (Model HR-S7300U, US JVC, Elmwood Park, NJ) at a rate of 30 frames per second throughout the entire experiment. A set of images from each experiment was digitized using a digital frame grabber system (Com- puterEyesPC1 version 2.00, Digital Vision, Dedham, MA).

Three regions of interest were established for each ligament and were defined by the stained lines bounding the region. The middle region was bounded by the lines immediately proximal and distal to the center line and accounted for approximately one-third of the length of the ligament. The femoral region was defined by the line at the distal end of the middle region and the line closest to the femur and repre- sented approximately one-sixth of the length of the ligament. The acetabular region was demarcated by the line at the proximal end of the middle region and the line closest to the acetabulum and also represented approximately one-sixth of the ligament length. The dis- tance between the stained lines bounding the region of interest was measured on each frame using image analysis software (Scion Image Release Beta 2, Scion, Frederick, MD).

Force at failure was measured as the highest load cell output during distraction of the ligament ends [32]. Stress was defined as distraction force divided by the initial cross-sectional area of the region of interest. Engineering strain was calculated by dividing the change in distance between the two lines bounding the region of interest by their original distance apart [2,32,35].

Stress and strain were then plotted for each set of frames for each ligament and region with stress on the x-axis and strain on the y-axis. A least-squares nonlinear regression curve in the form s = A(eB‘ - 1) was fit to the stress (s ) and strain ( E ) data for each ligament [2,26,35]. The strain energy density for each ligament and region was calculated as the area under the stress-strain curve. The tangent modulus in the toe region of the curve was determined from the slope at 0% strain. The tangent modulus in the linear portion of the curve was calculated from the slope at 80% of failure strain. This criterion was used since all of the specimens exhibited linear behavior in this portion of the stress-strain curve.

Poisson’s ratio (v) was calculated by dividing the negative transverse strain by the axial strain for each ligament’s set of frames. Transverse strain was measured at the center stained line and was calculated by dividing the change in width of the ligament by the original width. The resolution of the optical measurement system for these calculations was 3.4 x loe3 pixels per micron. Axial strain was calculated by dividing the change in distance between the two outermost stained lines by their original distance apart. Nega- tive transverse strain was plotted against axial strain for each liga- ment’s set of frames. The relationship between these two values was either linear or bi-linear. As a result, v was reported for two strain ranges that consistently exhibited linear behavior: 0-5% strain and 0.654.90 of failure strain.

A two-Factor analysis of variance model with repeated measures and a Newman-Keuls post hoc test was used to determine statistical differences among the three ligaments and three regions (Statistica for Windows Release 5.1, Statsoft, Tulsa, OK). Statistical significance was reported at the 95% confidence level ( P < 0.05).

Results

In general, the stress-strain response for the three regions of the hip capsule ligaments was nonlinear,

- 5 m a E4

5 2

i 3

1

0

A Acetabular

I r I t I

0 2 4 6 a 10 12

Strain (%)

Fig. 3. Sample least-squares nonlinear regression curves for the ace- tabular, middle and femoral regions of an iliofemoral ligament. The ligaments exhibited nonlinear behavior well described by an expo- nential stress-strain law, s =A(eB‘ - 1). R2 is 0.95, 0.94 and 0.97, re- spectively.

showing an initial “toe”region of lower modulus fol- lowed by an increase in modulus at higher strains (Fig. 3 ) . This nonlinear behavior was well described by an exponential curve with an average R’ for the non- linear regression curve fits of 0.87.

Five ischiofemoral ligaments failed in the midsub- stance, and five avulsed at the femoral bone block. Failure locations for the superior iliofemoral ligament included two in the midsubstance, three avulsions at the femur and five avulsions at the ilium. Of the inferior iliofemoral ligament, one failed in the midsubstance, two avulsed at the femur, and seven avulsed at the ilium.

The cross-sectional areas of the three ligaments and their respective regions are shown in Table 1. The cross- sectional area of the three ligaments differed significantly with regard to ligament (P < 0.05). In particular, the cross-sectional area of the ischiofemoral ligament was significantly lower than that of the superior iliofemoral ligament (P < 0.05).

Significant differences were found in engineering strain at failure of the bone-ligament-bone structure among the different ligaments (Table I , P < 0.05) and regions (P < 0.000001). The superior iliofemoral liga- ment had significantly lower strain values at failure than the ischiofemoral ligament (P < 0.05), and there was a trend towards the inferior iliofemoral being less than the ischiofemoral. The femoral region showed significantly greater strain at failure than both the acetabular and middle regions (P < 0.0005).

No significant differences were found for the failure stress with respect to ligament or region (Table 1 ) .

The modulus of elasticity of the stress-strain curve was reported at OYO (toe region) and 80% of failure strain (linear region) (Table 1). In the toe region, no significant differences were observed. In the linear portion of the

362 J. Hekvitt et al. I Journal of Orthopaedic Rrseurch I 9 (20011 3.59-364

Table 1 Regional mechanical properties of the superior iliofemoral, inferior iliofemoral and ischiofemoral ligaments - mean (S.D.)

Superior Inferior Ischiofemoral, iliofemoral, iliofemoral, n = I0 I7 = 10 n = 10

Cross-stjctionul urtw (mm' .4cetabular I 50 (1 30) 100 (52) 63 ( 5 5 ) Middle 120 (40) 92 (48) 81 (38) Femoral 99 (39) 89 (50) 79 (40)

.Strain U I structurd fhilurr 4cetabular 8.51;1 I 1 .@!,<I 7.8'Ch (4.04 0 )

( 3.3":,)" (6.7" 0)

Middle 6.2',,1 10.4?,,, 8. I '! , I ( 3.7%) ( I .8~!~,!)~ (4.7"h)

Femoral I3.3':u 1 1.4% 25.3"v (7.5";n)h ( 5.0%,)" ,b (3.3%)"

Strcss at structurul juilure (h1Pu) Acetabular 3.3 (2.0) 6.1 (7.4) 2.4 (2.0) Middle 1.7 ( I 4) 6.2 (8.8) 2.0 (1.4) Femoral 2.7 ( I .6) 6.1 (9.4) 3.5 (2.4)

h1odulu.s c?f' c~la.sti~ity ui O',O o/'./hilurc strain ( hIPa) Gcetabular 3.2 (3.4) 3.0 (3.1) 4.8 (7.0) Middle 1.9 (1.5) 3.3 (5.4) 3.9 (5.7) Femoral 1.0 ( 1 . 0 ) 2.2 ( I .9) 2.1 (2.1)

h1otlulu.s of'elustiitity (it 80"A of',fhihm struin ( MPu) Acetabular 112.9 285.8 80.9 (68.4)

Middle 113.3 242.2 99.5 (116.1)'

Femoral 76.1 (57.3) 139.3 82.1 (97.9)

Strain energy ilen.sity (MPir) Acetabular 0.10 (0.09) 0.32 (0.43) 0.04 (0.04) Middle 0.05 (0.03) 0.19 (0.25) 0.07 (0.09) Femoral 0.13 0.20 0.51 (0.39)d.'

(70.6) (390.5)

(63.6)' (419.9)'

(174.4)

(O.ll)d (0.37)d' a P < 0.05 for superior iliofemoral vs. ischiofemoral.

P < 0.0005 for femoral vs. acetabular and middle. ' P < 0.05 for middle vs. femoral. P < 0.005 for femoral vs. acetabular. P < 0.0005 for femoral vs. middle.

stress-strain curve, a statistically significant effect of ligament region was detected ( P < 0.05). Specifically, the middle region had significantly higher moduli of elas- ticity than the femoral region ( P < 0.05).

A statisticaHy significant difference was observed in the strain energy density at failure with respect to region ( P < 0.0005) (Table 1). The femoral region exhibited significantly higher strain energy density compared to the acetabular ( P < 0.00s) and middle ( P < 0.OOOS) re- gions.

The Poisson's ratio (11) was observed to be either linear or bi-linear with strain and was reported at 0-5% strain and at 65-90% of the failure strain (Table 3). No significant differences were found between ligaments for either of these measures of v.

Table 2 Average Poisson's ratio ( L,) for superior iliofemoral. inferior iliofe- moral and ischiofemoral - mean (S.D.)

Superior Inferior Ischiofe- iliofemoral, iliofemoral, moral, n = 10 n - I 0 n - 1 0

Average Y from 1.3 (0.5) 1.1 (0.9) 2.0 (1.9) 0-5",;1 strain Average 11 from 1.3 (0.5) 1.4 (0.5) 1.4 (0.9) 65 90'!,11 of failure strain

Discussion

This study presents a detailed mechanical analysis of the material properties of the major hip capsule liga- ments: the iliofemoral ligaments and the ischiofemoral ligament. Our results indicate that significant differences exist in the material properties of these ligaments as well as between their respective regions. These findings sug- gest that specific material as well as structural differences exist in the ligaments of the hip joint capsule.

The failure strain was significantly lower for the an- teriorly located iliofemoral ligaments than the posteri- orly located ischiofemoral ligament. This finding is consistent with structural strain at failure previously reported by this group as 25.6 & 9.5'%, for the ischiofe- moral ligament, 17.0 f 5.6% for the superior half of the iliofemoral ligament and 18.9 & 5.4% for the inferior half [13].

While failure stress was not significantly different between the ligaments, the greater cross-sectional area of the iliofemoral ligaments means that they could withstand greater force overall than the ischiofemoral ligament. This conclusion is supported by structural measurements of maximum force at failure previously reported. The ischiofemoral ligament withstood 136.0 * 74.6 N before failing while the superior and inferior halves of the iliofemoral ligament withstood 320.3 31 267.7 N and 351.3 * 159.4 N, respectively [13]. These observations suggest that the mechanical prop- erties of the hip capsule may contribute to the lower incidence of anterior dislocation of the hip (10-15% of hip dislocations) compared to posterior dislocation (85-90% of hip dislocations) 171.

The failure strain also differed significantly with re- gard to the region of the ligament. The femoral region of the ischiofemoral ligament is the narrowest portion of the ligament and showed 2-3 times greater strain at failure than the other regions. This focal area of in- creased strain could represent an area predisposed to posterior subluxation and dislocation. The variation in strain across ligament regions is consistent with regional strain variation found by Woo and colleagues [32]. This variation may be due to heterogeneity of the biochemi- cal components of the ligaments between regions [10,38].

J. Hrivitt et al. I Journal of Orthopirrdic Rrsrurrh 19 (2001 ) 359-364 363

While there is no comparative data in the literature on the mechanics of the hip capsule, there is a consid- erable body of information on the mechanics of the shoulder capsule. Bigliani et al. [2] reported maximum stress of 5.5 f 3.2 MPa for the inferior glenohumeral ligament of the shoulder joint capsule. Ticker and col- leagues [26] reported maximum stress of 7.7 + 2.5 MPa for the same ligament. Itoi et al. [14] reported maximum stress ranging from 8.1 f 3.3 MPa to 21.3 f 5.7 MPd for the four quadrants of the shoulder joint capsule. These values are generally higher than the failure stress values of 2.0-6.2 MPa reported here for the hip joint ligaments.

Mid-substance strain of 10.9 * 5.5%) for the inferior glenohumeral ligament was reported by Bigliani et al. while Ticker et al. reported mid-substance strain to be 9.3 6 3.1Y0 for the same ligament [2,26]. These values fall within the failure strain values of 6.2-25.3’34 presented in this study for the hip joint ligaments.

Tensile modulus in the linear region of the stress- strain curve was reported by Ticker et al. [26] to be 103.5 rt 36.8 MPa for the inferior glenohumeral liga- ment. Bigliani et al. 131 reported the tensile modulus of the same ligament to be 36.9 ik 14.6 MPa. Itoi et al. [14] reported tensile modulus ranging from 31.5 f 9.4 MPa to 66.9 * 2.4 MPa for the four quadrants of the shoul- der joint capsule. These values are generally lower than the moduli of elasticity of 76.1-285.8 MPa reported here. The results suggest that the overall material be- havior and properties of the ligaments of different joint capsules are similar but not identical.

Despite the similarity in material properties between the hip and shoulder joint capsule ligaments, the hip joint ligaments have substantially greater cross-sectional area than the shoulder joint capsule ligaments [2,14,26]. Thus, the hip joint capsule is able to withstand greater tensile force than the shoulder joint capsule. This dif- ference, in addition to differences in the bony anatomy of the two joints, may contribute to the greater clinical incidence of shoulder dislocation as compared to hip dislocation.

The Poisson’s ratio (11) is required to fully describe the tensile properties of the hip ligaments in tension, but to our knowledge it has not previously been re- ported. While the Poisson’s ratio did not differ sig- nificantly with respect to ligament, the values of 11

reported here are significantly greater than 0.5 pro- viding evidence for the expected anisotropic properties of ligament. These values are also consistent with 11

reported for other anisotropic connective tissues in tension: anulus fibrosus ( v = 1.63), articular cartilage ( v E’ 3.3) and mensicus ( v = 1.59-2.32) [1,9,23]. In a poroelastic, or biphasic material, the Poisson’s ratio will also influence the flow of interstitial fluid in re- sponse to mechanical stress, which in turn may regu- late the viscoelastic behavior of the tissue [5,17]. In

this regard, the Poisson’s ratio may play an important role in governing mechanical behavior of ligamentous tissues.

In this study, very low strain rates were used in order to minimize viscoelastic effects of the ligaments. Stiffness of bone-ligament-bone specimens has been shown to increase with increased strain rates [34]. Thus, the stiffness of the hip joint capsule ligaments would be expected to increase at high physiologic strain rates, such as those associated with motor ve- hicle trauma or sports injuries. The mechanical prop- erties of the hip joint capsule as defined in this study can be used as baseline data to study the strain rate dependent properties of the ligaments at more physio- logic strain rates.

The mechanical profile of the ligaments of the hip capsule has clinical relevance to hip joint stability. Un- derstanding which regions of a capsular ligament con- tributes most to hip joint stability will help in deciding which structures to avoid or to repair during a surgical approach in order to minimize complications related to hip joint instability. Knowledge of the mechanical properties of the hip joint ligaments will also assist in designing strategies to repair the capsule after traumatic injury.

The incidence of hip dislocation following total hip arthroplasty is approximately 3% [12]. Up to 70%) of these dislocations occur four to five weeks after surgery and are most commonly the result of soft tissue laxity prior to the healing of the pseudocapsule [lS]. It has been suggested that repair and proper tensioning of the hip capsule after total hip arthroplasty can reduce soft tissue laxity and potentially decrease the incidence of early dislocation after surgery. Knowledge of the me- chanical properties of the hip joint capsule may prove useful in the treatment of these problems and may fa- cilitate the development of new techniques and materials for capsular repair.

In summary, this study represents a first step in de- fining the mechanics of the hip joint capsule ligaments. Determination of the mechanical properties of the shoulder joint capsule has broadened the understanding of shoulder instability and enhanced the treatment of this debilitating condition. This study on the mechanical properties of the hip joint ligaments could similarly en- hance the understanding of the role played by the joint capsule in hip stability and could ultimately help im- prove the treatment available for hip joint capsule pa- thology.

Acknowledgements

Funding provided by the Virginia Flowers Baker Endowment and an unrestricted research grant from Johnson and Johnson P.1.

361 J. HewGtt et al. I Journal of Orthopedic, Research 19 (2001 359-364

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