The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 84, Issue 1

Scientific Article | January 01, 2002

A Gender-Related Difference in the Contribution of the Knee Musculature to Sagittal-Plane Shear Stiffness in Subjects with Similar Knee Laxity

Edward M. Wojtys, MD; James A. Ashton-Miller, PhD; Laura J. Huston, MS

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Investigation performed at the Department of Orthopaedic Surgery, MedSport, University of Michigan, Ann Arbor, Michigan

Edward M. Wojtys, MD
Laura J. Huston, MS
Department of Orthopaedic Surgery, MedSport, 24 Frank Lloyd Wright Drive, Ann Arbor, MI 48106. E-mail address for E.M. Wojtys: edwojtys@umich.edu

James A. Ashton-Miller, PhD
Biomechanics Research Laboratory, Department of Mechanical Engineering and Applied Mechanics, Department of Biomedical Engineering, and Institute of Gerontology, University of Michigan, Ann Arbor, MI 48109

The authors did not receive grants or outside funding in support of their research or preparation of this manuscript. They did not receive payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, educational institution, or other charitable or nonprofit organization with which the authors are affiliated or associated.

J Bone Joint Surg Am, 2002 Jan 01;84(1):10-16

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Abstract

Background: Women’s susceptibility to injuries involving the anterior cruciate ligament remains unexplained. Volitional contraction of the knee musculature is known to increase the resistance of the knee to shear deformation, raising the possibility that muscles play a part in protecting the anterior cruciate ligament during hazardous activities. We therefore tested the hypothesis that a volitional co-contraction of the knee muscles increases the sagittal-plane shear stiffness (or resistance to anterior tibial translation) of the knee more in men than in women.

Methods: Twenty-three volunteers (ten men and thirteen women; mean age, 24.7 ± 5.4 years), all with anterior tibial translation of 6 mm, agreed to participate in the study. Each subject underwent a subjective evaluation of knee function and activity level, an arthrometric measurement of passive anterior tibial translation, and an isokinetic dynamometer strength test at 60Â°/sec. A dynamic stress test was then performed to measure anterior tibial translation while simultaneously monitoring lower-extremity muscle response.

Results: Maximum co-contraction of the knee musculature significantly decreased mean anterior tibial translation in both men and women (from 7.8 mm to 2.2 mm in men and from 6.5 mm to 3.1 mm in women). The corresponding percentage increase in shear stiffness of the knee was significantly greater (p = 0.003) in men (379%) than in women (212%).

Conclusions: The results suggested that women have a diminished potential for muscular protection of passive structures of the knee in anterior tibial translation.

Clinical Relevance: Maximal muscular protection of the anterior cruciate ligament in women may be less than that in men. This may be one factor explaining why more women than men are apt to sustain injuries to the anterior cruciate ligament.

Figures in this Article

Introduction

Introduction | Materials and MethodsSubjects | Results | Discussion | References

Female athletes are at greater risk for injuries involving the anterior cruciate ligament than are their male counterparts^1-6. Causal factors that have been implicated include the gender-related difference in Q-angle⁷, knee morphology^8-15, pelvic dimensions⁷, hormonal status^16-19, and athletic training^20-22. However, no one factor or combination of factors examined to date has provided a reasonable explanation for the gender-related difference in the risk of injury to the anterior cruciate ligament. Because gender-related differences in passive structures seem unlikely to provide a reasonable explanation, we explored the hypothesis of a gender-related difference in the active muscular protection of the passive structures of the knee.

The sagittal-plane shear stiffness of the knee is a measure of the resistance exerted by the soft-tissue structures of the knee in reaction to a force causing anterior tibial translation relative to the femur. Of particular interest is the temporary increase in stiffness that occurs during volitional activation of the muscles surrounding the knee²³. We did not consider changes in knee-joint stiffness caused by any pathological processes (for example, an injury, surgery, or degeneration).

Let us assume that an external force and/or moment forcibly displaces the tibia anteriorly relative to the femur, thereby threatening injury to the anterior cruciate ligament due to excessive tensile strain in that structure. Because both passive and active structures span the knee joint, both can potentially contribute to the stiffness resisting that tibial displacement, depending on the magnitude of the external force applied²³. However, when the subject volitionally tenses the knee muscles, the stiffness of those muscles increases (see Discussion), thereby stiffening the knee joint. For example, Markolf et al. showed that, by volitionally co-contracting the knee muscles, healthy adults could more than double the overall stiffness of the knee, thus resisting anterior tibial translation²⁴. This increase in muscle stiffness is important in that, hypothetically, it should help to protect the anterior cruciate ligament from excessive strain by reducing the proportion of the external force that must be resisted by the anterior cruciate ligament and other passive structures of the knee.

Because proportionately more injuries of the anterior cruciate ligament occur in women than in men, we hypothesized that the maximum contribution of the knee musculature to knee stiffness in resisting anterior tibial translation may be less in women than in men. If so, this suggests that the muscular protection of the knee joint in women may be less than that in men. The null hypothesis was that there was no gender-related difference in the anterior shear stiffness of the knee joint as measured with muscles relaxed or in a fully contracted state.

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Fig. 1:: Schematic drawing of knee-testing device used to measure anterior tibial translation while simultaneously monitoring the activity and responses of the lower-extremity muscles.

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Fig. 1:: Comparison of external load-displacement data with those of Markolf et al.²⁴. Stiffness is defined as the slope of each curve.

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TABLE I: Gender Comparisons of Knee-Joint Stiffness, Muscle Strength, and Time Needed to Reach Peak Muscle Torque

*The values are given as the mean and the standard deviation. †P value is significant at p = 0.007 level.

	Men*	Women*	P Value
Anterior tibial translation (mm)
Passive	?????7.8 ± 2.1	?6.5 ± 2.8	0.03
Active	?????2.2 ± 1.5	?3.1 ± 1.8	0.001†
Sagittal-plane shear stiffness (N/mm)
Passive	??18.7	??19.3	0.71
Active	??70.9	??40.7	0.005†
% increase with muscle contraction	?379	?212	0.003†
Peak muscle strength (ft-lb/lb body weight)
Quadriceps	??89 ± 10	??69 ± 14	0.001†
Hamstrings	??45 ± 7	??37 ± 8	0.018
Time needed to reach peak muscle torque (msec)
Quadriceps	?412 ± 143	?419 ± 123	0.263
Hamstrings	?383 ± 157	?488 ± 167	0.144

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TABLE I: Gender Comparisons of Knee-Joint Stiffness, Muscle Strength, and Time Needed to Reach Peak Muscle Torque

*The values are given as the mean and the standard deviation. †P value is significant at p = 0.007 level.

	Men*	Women*	P Value
Anterior tibial translation (mm)
Passive	?????7.8 ± 2.1	?6.5 ± 2.8	0.03
Active	?????2.2 ± 1.5	?3.1 ± 1.8	0.001†
Sagittal-plane shear stiffness (N/mm)
Passive	??18.7	??19.3	0.71
Active	??70.9	??40.7	0.005†
% increase with muscle contraction	?379	?212	0.003†
Peak muscle strength (ft-lb/lb body weight)
Quadriceps	??89 ± 10	??69 ± 14	0.001†
Hamstrings	??45 ± 7	??37 ± 8	0.018
Time needed to reach peak muscle torque (msec)
Quadriceps	?412 ± 143	?419 ± 123	0.263
Hamstrings	?383 ± 157	?488 ± 167	0.144

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TABLE II: Comparison of Muscle Activation Levels (as a Percentage of a Maximum Voluntary Contraction) by Gender*

*No significant differences were found. †The values are given as the mean and the standard deviation.

Muscle	Relaxed Test†		Tensed Test†
Men	Women	Men	Women
Gastrocnemius	?7 ± 1	?7 ± 2	53 ± 6	49 ± 4
Lateral hamstring	?8 ± 1	?7 ± 1	73 ± 4	65 ± 7
Medial hamstring	?6 ± 1	?6 ± 1	82 ± 5	74 ± 7
Lateral quadriceps	13 ± 2	12 ± 1	65 ± 6	70 ± 5
Medial quadriceps	11 ± 2	12 ± 2	61 ± 7	65 ± 5

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TABLE II: Comparison of Muscle Activation Levels (as a Percentage of a Maximum Voluntary Contraction) by Gender*

*No significant differences were found. †The values are given as the mean and the standard deviation.

Muscle	Relaxed Test†		Tensed Test†
Men	Women	Men	Women
Gastrocnemius	?7 ± 1	?7 ± 2	53 ± 6	49 ± 4
Lateral hamstring	?8 ± 1	?7 ± 1	73 ± 4	65 ± 7
Medial hamstring	?6 ± 1	?6 ± 1	82 ± 5	74 ± 7
Lateral quadriceps	13 ± 2	12 ± 1	65 ± 6	70 ± 5
Medial quadriceps	11 ± 2	12 ± 2	61 ± 7	65 ± 5

Materials and MethodsSubjects

Introduction | Materials and MethodsSubjects | Results | Discussion | References

A power analysis based on preliminary data showed that eight men and eight women were needed to achieve statistical significance (alpha £ 0.05; power 0.80). After receiving approval from our Institutional Review Board to perform this study, we enlisted and obtained signed consent forms from twenty-three volunteers, ten men (mean age [and standard deviation], 25.0 ± 6.2 years; mean height, 1.80 ± 0.08 m; and mean weight, 79 ± 8 kg) and thirteen women (mean age, 24.5 ± 5.0 years; mean height, 1.68 ± 0.08 m; and mean weight, 64 ± 10 kg). The participants had no history of knee injury. To decrease the effect of anterior tibial translation as a confounding variable, we required the subjects to have loose but healthy knees; the maximum manual anterior arthrometric laxity measurement for each participant had to be at least 6 mm. Thirteen men and nine women did not meet this inclusion criteria and were thus excluded from the study. Activity levels ranged from sedentary to elite-level, reflecting the population that presents with anterior cruciate ligament tears.

Testing

Each subject underwent a subjective evaluation of knee function²⁵ and physical activity level, arthrometric measurement of anterior tibial translation (KT1000; MEDMetric, San Diego, California), isokinetic dynamometer strength testing at 60Â°/sec (Biodex Medical Systems, Shirley, New York), and dynamic anterior tibial translation stress testing (Fig. 1).

Knee-Testing Apparatus

The testing device was developed to record anterior tibial translation while simultaneously monitoring lower-extremity muscle response by means of surface electromyography²⁶. Anterior tibial translation was measured by ascertaining the difference between anterior displacements recorded by two linear potentiometers: one placed on the patella, and the other placed on the tibial tuberosity. Lower-extremity muscle function was quantified with the use of surface electromyography recording over five muscles: the lateral and medial quadriceps, the lateral and medial hamstrings, and the gastrocnemius. Patients were seated with the knee flexed 30Â° and the foot fixed in 10Â° to 15Â° of ankle dorsiflexion. The weight-bearing status of the limb was monitored by a scale under the foot, and the scale was maintained in the range of 9 to 14 kg of force (kg-f). A constant test force was then abruptly applied to the posterior aspect of the proximal part of the calf (rate = 1483 N/sec). The magnitude of that force was held at 20% of the subject’s body weight. For example, an 89-N shear force was applied to a subject weighing 45 kg-f, and a 179-N force was applied to a subject weighing 91 kg-f.

Electromyographic recordings were sampled at a frequency rate of 1 kHz during a 2.5-second window of time, beginning 0.5 second before the onset of the anteriorly directed test force.

Testing Protocol

After an orientation session during which the anteriorly directed test force was applied several times, two types of tests were run. In the relaxed test, subjects were asked not to contract the quadriceps, hamstrings, or gastrocnemius muscles in response to the anteriorly directed force. Comparison of electromyographic levels in the fully relaxed state was used to confirm muscle inactivity. In the tensed test, subjects were instructed to exert maximum co-contraction of the muscles around the knee to resist the anteriorly directed force prior to the application of that force. Comparison of electromyographic levels with maximum voluntary contraction was used to confirm maximum co-activation. Ten normalized step-force trials (ten with relaxation and ten with contraction of the muscles) of each test condition were applied to each subject, and the results were averaged.

Level of Muscle Activation

The percentage of muscle activation was defined during a test as the percentage of the maximum voluntary contraction of each of the five muscle groups studied (the lateral and medial quadriceps, lateral and medial hamstrings, and gastrocnemius). The level of muscle activation was determined for the stiffness tests conducted with both relaxed and fully activated muscles.

Data Analysis

Knee (secant) shear-stiffness values were obtained by dividing the load of the anteriorly directed step force by the anterior displacement of the knee joint. The maximum percentage increase in knee-joint stiffness caused by volitional muscle activity was then calculated as the anterior tibial translation in the relaxed state divided by the anterior tibial translation in the contracted state, multiplied by 100.

Statistics

Descriptive statistics were calculated for all variables. A repeated-measures analysis of variance was used to test the null hypothesis that gender had no effect on the percentage change in knee-joint stiffness. Post hoc t tests were used to test the magnitude and direction of any main effects with use of an initial alpha level of 0.05. However, this p value was adjusted down by the number of multiple comparisons involved (significance reached at p = 0.007). A multiple linear regression model was used to determine the relative contributions of the independent variables (gender, height, and strength) to the dependent variable of sagittal-plane shear stiffness.

Results

Introduction | Materials and MethodsSubjects | Results | Discussion | References

Effect of Leg Dominance

There were no significant differences in shear stiffness of the knee, muscle strength of the quadriceps and hamstrings, or time needed to reach peak muscle torque (time to peak torque) between the dominant and the nondominant lower extremity. Therefore, all reported values were for the dominant leg only.

Sagittal-Plane Knee Stiffness

(Table I)

Effects of Gender

There were no significant differences in either passive knee laxity or shear stiffness between men and women (Table I; p = 0.71). The male volunteers exhibited a mean anterior tibial translation of 7.8 mm and an average passive shear-stiffness value of 18.7 N/mm in the relaxed muscle state, whereas the female volunteers exhibited a mean anterior tibial translation of 6.5 mm and an average passive shear-stiffness value of 19.3 N/mm. Maximum co-contraction of the knee musculature significantly decreased the mean anterior tibial translation in both men and women (to 2.2 mm in men and to 3.1 mm in women; p = 0.001). Correspondingly, the men produced significantly higher stiffness values than did the women (70.9 N/mm compared with 40.7 N/mm; p = 0.005). In other words, the men were able to increase knee-joint stiffness significantly more than the women could (379% compared with 212%; p = 0.003). Interestingly, no gender-related differences in the levels of athletic activity were found (6.2 of 10 for men compared with 4.9 of 10 for women; p = 0.17).

Association Between Sagittal-Plane Knee Stiffness and Muscle Strength

Even though men exhibited significantly higher peak torques in both the quadriceps and the hamstrings (Table I), the multiple regression analysis showed that muscle strength per se was not the predominant contributor to sagittal-plane knee stiffness: stiffness = —0.009(x1) — 17.777(x2) + 0.517(x3) + constant, where stiffness = absolute value of maximum stiffness, x1 = muscle strength (p = 0.974), x2 = gender (p = 0.049), x3 = subject’s height (p = 0.666), constant = 51.976 (p = 0.576), and r² = 0.68.

The ability to increase anterior knee stiffness was not determined by muscle strength or body height, but primarily by gender (p = 0.049).

No significant difference in the electromyographic activation level (percentage of maximum voluntary contraction) in the gastrocnemius, quadriceps, or hamstring muscles was found between men and women (Table II).

Muscle Strength

(Table I)

Gender-Related Factors

The male volunteers produced significantly higher quadriceps peak torque values compared with the female volunteers in this study (89 ft-lb/lb of body weight for men compared with 69 ft-lb/lb of body weight for women; p = 0.001). Similarly, hamstring strength was greater in the men than in the women (45 ft-lb/lb of body weight for men compared with 37 ft-lb/lb of body weight for women; p = 0.018).

Time to Peak Torque

(Table I)

No correlation was found between the time to peak torque of either the quadriceps or the hamstrings and increased knee stiffness in the sagittal plane (quadriceps, r² = 0.19; hamstrings, r² = 0.14). Although no significant difference was found in time to peak torque between the men and women in this study (Table I), the hamstrings of the men tended to respond faster to anterior tibial translation than did those of the women (383 msec compared with 488 msec; p = 0.144).

Discussion

Introduction | Materials and MethodsSubjects | Results | Discussion | References

The novel finding in this study was that the women could increase shear stiffness of the knee significantly less than the men could. Female volunteers could double the shear stiffness of the knee between the passive and active muscle states, suggesting that the portion of muscle stiffness provided by active muscle co-contraction was approximately equal to the total stiffness developed through deformation of passive tissues and resting muscles. The male volunteers, on the other hand, could more than triple the resting shear stiffness of the knee with volitional knee muscle co-contraction. This finding implies that, in the men, active knee muscles provided twice as much resistance to shear deformation as the passive structures and resting muscles combined.

The present values of sagittal-plane knee stiffness agree with previous values reported in the literature. At a test force of 100 N to translate the tibial plateau anteriorly with respect to the femur, Markolf et al. recorded an average of 3.7 mm of anterior tibial translation in the knees of cadavers²³. This experiment quantified the passive tissue stiffness without any contribution from the muscles. In vivo, in relaxed volunteers, Markolf et al. recorded an average of 5.5 mm of anterior tibial translation under 100 N of force at 20Â° of knee flexion²⁴, whereas we recorded an average of 7.2 mm at 30Â° of knee flexion (Fig. 2). In volunteers with fully activated knee musculature, Markolf et al. recorded an average anterior tibial translation of 1.96 mm, whereas we recorded an average of 2.0 mm (range, 1.6 to 2.3 mm). Hence, the present values, obtained with testing methods slightly different from those of Markolf et al., are consistent with their values. This comparison also indicates that, on the average, the passive tissues of the knee develop approximately two-thirds of the total knee stiffness seen in vivo in the resting state. It is noteworthy that previous investigations of the passive determinants of joint stiffness indicated that approximately 40% to 50% of this parameter is determined by muscle^27,28. So, even in the resting state, muscle contributes appreciably to the knee’s ability to resist anterior tibial translation.

The tensile stiffness of a single muscle is dependent on several factors: (1) the level of muscle activation, which determines the number of bound cross-bridges^29,30 and therefore the total force developed by the muscle; (2) the cross-sectional area and pennation angle of the muscle fibers; (3) the amount and arrangement of passive connective tissue in the muscle; (4) the imposed change in muscle length, which determines whether the short-range stiffness of the cross-bridges will be exceeded³¹; (5) the velocity of the imposed change in muscle length, which determines whether cross-bridge cycling will have an effect³²; and (6) tendon stiffness^33,34. The shear stiffness of the knee is likely also to depend on the number and identities of the actively contracting muscles that span the joint. The overall level of muscle activation was the only variable that was directly assessed in the present investigation, and this is discussed below and in Table II. The contribution of the gamma motoneuron system to stiffness of the knee joint through the reflex regulation of the lengths of the quadriceps, hamstrings, and gastrocnemius could not be documented^35-38.

A voluntary muscle response initiated at the onset of an external force at the knee joint can, in a situation of severe impact, be too slow to increase joint stiffness and thereby prevent a ligamentous injury^39,40. If, however, the muscles are already contracted either because of other functional demands prior to the application of the deforming force or because of volitional co-contraction, then the inherent increase in stiffness that accompanies that muscle contraction will help to protect the knee at impact. An example of another functional demand is the need for the quadriceps to contract prior to landing on a stance limb so that it can develop sufficient rotational stiffness to prevent the knee from buckling (flexing and giving way) during the impact of landing. This is a familiar illustration of how the muscle stiffness of the knee is automatically preset prior to landing from a jump^41-43. Should the hamstrings also be co-activated during this landing maneuver, they will help to resist tibial translation relative to the femur in the same manner as was recorded under sedentary conditions by Markolf et al.²⁴ and in the present study. The degree of difficulty of a task probably helps to determine how much antagonist muscle activity is needed to stabilize the joint^44-47, thereby affecting the shear stiffness developed in the knee. It is not known whether men and women co-activate knee muscles differently in athletic maneuvers that place the knee under shear loading.

In this study, women did not generate the levels of shear stiffness per unit of body weight that men did. Levels of muscle activation were compared between men and women to determine if men and women used the muscles similarly to stiffen the knee to the same degree (Table II). Even though no significant differences were found in activation level between men and women, interesting trends were noted. In response to the induced anterior tibial translation, the women activated the quadriceps to a greater degree than did the men, whereas the men activated the hamstrings to a greater degree than did the women. From a biomechanical perspective, increased activation of the hamstrings decreases the strain on the anterior cruciate ligament, whereas increased quadriceps activity increases the strain on the anterior cruciate ligament for knee flexion angles up to 60Â°.

In considering the clinical implications of this study, it is useful also to consider the limitations of the study. One limitation is that the men and women were not matched according to size, and therefore the men had larger muscles and larger passive knee structures than did the women. It is not known whether men and women of similar body size have similar knee stiffness properties. A second limitation of this study is that we cannot be certain that the increase in measured sagittal-plane knee stiffness always reflects a corresponding increase in protection of the anterior cruciate ligament without imparting any additional strain to that ligament. This issue would have to be resolved by direct measurement of the strain on the anterior cruciate ligament. The third limitation of this study is that, although the self-reported physical activity levels did not differ significantly between the men and women, the individuals had varied levels of athletic participation. Although a torn anterior cruciate ligament is a common injury in this population, the use of a more homogeneous group of athletes might have reduced some of the variability in these data. A fourth limitation of this study is that the stiffness determinations were performed only in the sagittal plane. Many anterior cruciate ligaments are torn in axial rotation, which was not addressed here, and the contribution of the knee muscles to rotational stiffness of the knee is not known. Although the number of individuals tested was justified by the power analysis, the use of a larger number of subjects more homogeneously grouped by age and physical activity might better determine if the results of this study represent a generalized phenomenon or are more pertinent to certain subgroups. Finally, we believe that some selection bias was introduced by comparing men with anterior tibial translation of 6 mm with a normal distribution of women. This bias was used in an effort to eliminate anterior tibial translation as a confounding variable. Despite this biased selection, we believe that the results and conclusions are still valid for the groups represented by the subjects tested.

Because of the gender-related differences detected in this study, we believe that the smaller maximum increase in knee-joint stiffness in women could be a factor in the increased prevalence of injury to the anterior cruciate ligament in female athletes. Should this finding be corroborated by others, further investigation will be needed to determine whether this deficiency is correctable with muscle-training or conditioning.

In conclusion, the ability to increase knee-joint stiffness in response to an external force causing anterior tibial translation was found to be gender-dependent in this sample of knees with 6 mm of anterior tibial translation. Translational knee-joint stiffness does not appear to be directly determined by muscle strength, body weight, or height.

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Topics

knee region ; knee joint ; multiple endocrine neoplasia ; tibia ; torque ; leg ; gender ; women ; stiff knee ; posterior muscle of thigh

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Edward M. Wojtys, James A. Ashton-Miller, Laura J. Huston; A Gender-Related Difference in the Contribution of the Knee Musculature to Sagittal-Plane Shear Stiffness in Subjects with Similar Knee Laxity. The Journal of Bone & Joint Surgery. 2002 Jan;84(1):10-16.

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