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Relationships of hamstring muscle volumes to lateral tibial slope
THEKNE-02536; No of Pages 7 The Knee xxx (2017) xxx–xxx
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The Knee
Relationships of hamstring muscle volumes to lateral tibial slope☆ Randy J. Schmitz a,⁎, Anthony S. Kulas b, Sandra J. Shultz a, Justin P. Waxman e, Hsin-Min Wang c, Robert A. Kraft d a
The University of North Carolina at Greensboro, Greensboro, NC, United States East Carolina University, Greenville, NC, United States c China Medical University, Taichung, Taiwan d Wake Forest University, Winston-Salem, NC, United States e High Point University, High Point, NC United States b
a r t i c l e
i n f o
a b s t r a c t
Article history: Received 9 January 2017 Received in revised form 9 August 2017 Accepted 16 September 2017 Available online xxxx
Background: Greater posterior–inferior directed slope of the lateral tibial plateau (LTS) has been demonstrated to be a prospective ACL injury risk factor. Trainable measures to overcome a greater LTS need to be identified for optimizing injury prevention protocols.
Keywords: ACL injury Magnetic resonance imaging
Methods: Eleven healthy females (mean +/- standard deviation) (1.63 ± 0.07 m, 62.0 ± 8.9 kg, 22.6 ± 2.9 years) & 10 healthy males (1.80 ± 0.08 m, 82.3 ± 12.0 kg, 23.2 ± 3.4 years) underwent magnetic resonance imaging of the left knee and thigh. LTS, semitendinosus muscle volume, and biceps femoris long head muscle volume were obtained from imaging data.
It was hypothesized that Healthy individuals with greater LTS who have not sustained an ACL injury would have a larger lateral hamstring volume.
Results: After controlling for potential sex confounds (R2 = .00; P = .862), lesser semitendinosus volume and greater biceps femoris-long head volume were indicative of greater LTS (R2 Δ = .30, P = .008). Conclusions: Healthy individuals with greater LTS have a muscular morphologic profile that includes a larger biceps femoris-long head volume. This may be indicative of a biomechanical strategy that relies more heavily on force generation of the lateral hamstring and is less reliant on force generation of the medial hamstring. Level of evidence: Level IV. © 2017 Elsevier B.V. All rights reserved.
1. Introduction Biomechanical and neuromuscular factors have dominated the anterior cruciate ligament (ACL) injury risk-factor literature, as these risk factors seemingly have a relative ease of identification and potential for direct intervention and prevention. However, outcomes are mixed with regard to the effectiveness of screening movement biomechanics to predict injury risk [1–3]. A number of anatomical risk factors for ACL injury have been identified [4], but are often dismissed in prevention programming due to the perceived difficulty in modifying anatomical structure. As such, the development of interventions aimed to moderate injury risk in ☆ MRI data were obtained by support of the Gateway MRI Center at the University of North Carolina at Greensboro. ⁎ Corresponding author at: Dept. of Kinesiology, 256 Coleman, The University of North Carolina at Greensboro, Greensboro, NC 27402, United States. E-mail address: [email protected] (R.J. Schmitz).
https://doi.org/10.1016/j.knee.2017.09.006 0968-0160/© 2017 Elsevier B.V. All rights reserved.
Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006
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individuals with high-risk non-modifiable anatomical factors is of clinical importance for preventing knee injury and subsequent risk of early degenerative joint disease. The articular geometry of the knee is important in the transmission of joint loads and resultant movement biomechanics [5]. In this regard, posterior–inferior directed slope of lateral tibial plateau (LTS) has been increasingly studied as a potential risk factor [6]. A larger LTS has been associated with increasing ACL force during axial loading activities [7,8]. While both posterior medial and posterior lateral tibial plateau slopes can be obtained from magnetic resonance imaging (MRI) data, a larger LTS in combination with axial load is theorized to contribute to greater anterior tibial translation as well as greater internal tibial rotations [5], both of which are known to increase ACL strain [9]. Both retrospective [10] and prospective studies have identified a greater LTS as a risk factor for ACL injury [5] as well as a risk factor for re-injury to the ACL reconstructed knee [11]. While the structural nature of this risk factor cannot be easily modified, there is a need to consider ways that the surrounding musculature can be trained to either counteract or compensate for these structural variants. Thus, investigations of modifiable factors that may be related to such established anatomical risk factors are warranted. Given the agonistic relationship of the hamstrings to ACL function, available hamstring muscle volume (and subsequent force production capability) may be one means to counteract the mechanism by which LTS increases ACL strain and corresponding injury risk. Cadaver studies have demonstrated that the hamstrings' distal attachments on the proximal tibia and fibula allow this muscle group the ability to influence anterior–posterior displacement and internal–external rotation of the tibia relative to the femur [12– 15]. In addition, adequate co-contraction of the hamstrings has been shown to effectively reduce anterior translation and internal rotation of the tibia, thereby enhancing knee joint stability and reducing ACL strain [16–19]. As such, current ACL injury prevention and rehabilitation efforts often attempt to strengthen the hamstring muscle group as a whole in order to increase the net force applied by the hamstrings and thus enhance knee joint stability. However, given differential hamstring muscle function in the transverse plane [20], it may be of greater benefit to focus on the effects of individual hamstring muscle forces to reduce ACL loading. Although co-contraction of the hamstrings has been shown to effectively reduce anterior tibial displacement and internal tibial rotation [14,15], these findings have been established via symmetrical loading of the medial (i.e. semitendinosus and semimembranosus) and lateral hamstrings (i.e. biceps femoris short head and long head). Differences in morphological features that influence muscle force production such as muscle volume, pennation angle, physiological cross-sectional area, and muscle fiber length have been identified among different hamstring muscles [21,22]. In addition, it has been demonstrated that the lateral hamstring action is more influential on knee joint kinematics compared to medial hamstring action due a larger moment arm in the transverse plane [12,23]. It is possible that individuals with a steeper LTS may require a greater capacity for force production in the lateral hamstring musculature in order to better resist anterior tibial displacement and internal rotation. This in turn may protect the ACL from deleterious multi-planar loads. Thus the purpose of this study was to determine the relationship of individual medial and lateral hamstring muscle volumes to LTS. It was hypothesized that healthy individuals with greater LTS who have not sustained an ACL injury would have a larger lateral hamstring volume. Testing of the healthy individuals allows us to better determine muscular targets for future training/intervention work. 2. Materials and methods 2.1. Experimental protocol Eleven healthy females (mean +/- standard deviation) (1.63 ± 0.07 m, 62.0 ± 8.8 kg, 23.6 ± 2.7 years) and 10 healthy males (1.80 ± 0.08 m, 82.3 ± 12.0 kg, 23.5 ± 3.8 years) attended one session in which they underwent MRI examination. Healthy was defined as no current orthopedic injury or history of significant injury or surgery in left limb. Height, weight, and age were obtained along with an MRI assessment of muscle volume and tibial geometry. All measures were obtained on the left limb (preferred stance limb in 18/21 participants). MRI examination of the left limb was performed with a three tesla MRI system (Trio, Siemens, Erlangen, Germany) using a 15 channel transmit/receive high resolution knee coil and a combined spine and body coil for the hamstring muscle volume measures. Tibial geometry measurements were acquired with T1-weighted fat suppressed sagittal MRI scans of the tibiofemoral joint (Slice Thickness = 0.6 mm, In-Plane Resolution = 0.5 mm × 0.5 mm, Number of Slices = 176, FoV = 320 × 320 mm, TR = 1200 ms, TE = 33 ms, Flip Angle mode = PdVar, Bandwidth (Hz/pixel) = 539 Hz. Fat Suppression = SPAIR. Acquisition time = 8:29). Muscle volume measurements were obtained with T1-weighted fat suppressed frontal MRI scans of the thigh (Slice Thickness = 1.0 mm, In-Plane Resolution = 3.0 mm × 3.0 mm, Number of Slices = 256, FoV = 480 × 480 mm, TR = 1200 ms, TE = 33 ms, Flip Angle mode = PdVar, Bandwidth (Hz/pixel) = 539 Hz. Fat Suppression = SPAIR. Acquisition time = 8:29). The resulting images allowed visualization of both the hip joint and knee joint. 2.2. Tibial slope measurement Using MIPAV software (http://mipav.cit.nih.gov), LTS was measured by a single examiner as described by Hudek et al. [24]. First, the central sagittal image was selected on which the tibial attachment of the posterior cruciate ligament (PCL), the intercondylar eminence, and the anterior and posterior tibial cortices appeared in a concave shape. Next, two circles (proximal and distal) were drawn in the proximal tibia. The proximal circle touched the anterior, posterior, and superior tibial cortex bone and the distal circle had to touch the anterior and posterior cortex border. A standardized relative distance between the proximal and distal circles was established as the center of the distal circle was placed on proximal circle circumference Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006
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(Figure 1). The longitudinal axis of the tibia was then defined by a line connecting the centers of two circles and was transposed to all slices. The articulation center of the lateral tibial compartment was selected from an axial view, and a line was connected between the most anterior and posterior points of the lateral tibial plateau using the sagittal view. LTS was then defined by the angle formed by orthogonal to the MRI-longitudinal axis and the tangent to the lateral plateau (Figure 2). A posteriorly–inferiorly sloping value was defined as positive. The single LTS examiner established between-day intratester reliability and precision by reassessing 12 participants separated by at least 48 h (intraclass correlation coefficient +/- standard error of measurement) (ICC2,1 ± SEM = 0.98 ± 0.4°). 2.3. Muscle volume measurement For the medial hamstring, the semitendinosus was selected due to its slightly larger internal rotation moment arm [20]. For the lateral hamstring, the long head of the biceps femoris was selected for its larger external moment arm [20], and because it is more susceptible to injury and dysfunction than the semimembranosus [25]. Additionally, the biceps femoris long head produces more force than the short head during early stance [26], a time in weight acceptance commonly associated with noncontact ACL injury [27]. Further, reduced activity of this muscle has been predictive of ACL injury [28]. A single investigator calculated muscle volumes from serial anatomical cross-sectional areas (CSAs) of the semitendinosus and long head of the biceps femoris muscles in 2.25 cm intervals from the lateral knee joint line to the ischial tuberosity for each individual hamstring muscle in Osirix v5.7.1 (Osirix Foundation, Geneva Switzerland). Additional CSAs were measured at the most proximal and distal ends of each of the muscles where muscle tissue could be visualized. For each muscle, the CSAs were plotted against femur length and then fitted with a cubic spline. Volumes of the semitendinosus and long head of the biceps femoris were then calculated as the area under the CSA vs. femur length curves [29,30]. The investigator established betweenday intratester reliability and precision by re-measuring the muscle volumes of 10 participants separated by at least 48 h (ICC2,1 range ± SEM range) (0.99–0.99 ± 1.5–1.6 cm3). 2.4. Statistical analyses A linear regression was used to predict LTS. To control for reported sex differences in LTS [31], sex was initially entered on the first step. Semitendinosus volume and biceps femoris-long head volume were entered in a forward stepwise manner on subsequent steps. 3. Results Descriptive data are presented in Table 1. After controlling for sex (R2 = .00; P = .862), lesser semitendinosus volume and greater biceps femoris-long head volume predicted greater LTS (R2 Δ = .30, P = .008) (Table 2). Both muscles were significant predictors in the final model. Notably there were relative increases in magnitudes of the partial correlations relative to the zero order correlations of semitendinosus volume to LTS and biceps femoris volume to LTS (− 0.20 to − 0.62 and .21 to .59,
Figure 1. Central sagittal image with center proximal (0) and distal (1) circles defined. The proximal circle touched the anterior, posterior, and superior tibial cortices while the distal circle had to touch the anterior and posterior cortices. The line connecting these two centers was defined as the longitudinal axis of the tibia.
Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006
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Figure 2. Central sagittal image of lateral tibial plateau. Lateral tibial slope (LTS) was defined as the angle formed by a line orthogonal to the longitudinal axis and a line tangent to the lateral tibial plateau.
respectively) in the final model (Table 3). A scatterplot of muscle volumes and LTS is found in Figure 3. The resultant prediction equation was: LTS = 5.81 − .849Sex − 0.035semitendinosus volume + 0.034biceps femoris long head volume. 4. Discussion A better understanding of modifiable factors that have the potential to compensate for or counteract known anatomical risk factors for ACL injury may lead to more focused and effective injury prevention efforts. In this regard, we undertook a study that aimed to determine the relationship of individual medial and lateral hamstring muscle volumes to the established ACL risk factor of LTS. Because muscle volume is commonly understood to be modified through training interventions that induce muscle hypertrophy, we may be able to effectively reduce ACL loading and subsequent ACL injury risk by counteracting the biomechanical effects of LTS during axial loading. The following discussion addresses potential mechanisms of interaction between bony geometry and individual hamstring muscle function. The current results suggest an overarching idea that individual muscles may adapt to bony geometry as individuals with greater LTS have lesser semitendinosus muscle volume and larger biceps femoris muscle volume. Because hamstring volume has been previously correlated to measures of strength [32,33], we have reason to believe that the volume measures are related to strength capacity. This suggests that healthy individuals with a bony geometry that predisposes them to internal rotation during axial loading of the knee joint [5] may have a resultant biomechanical strategy that relies more heavily on force generation of the biceps femoris to control internal tibial rotation and is less reliant on force generation of the semitendinosus muscle. The concept of individual muscle adaptations to a stimulus is supported through previous literature. Although not related to joint bony geometry, individual hamstring muscles adapt following ACL surgery [34]. In a follow-up study of patients who underwent ACL reconstruction with a hamstring tendon graft at least two years previously, there was a 7.7% larger biceps femoris long head volume in the surgical limb compared to the contralateral limb [34]. The authors suggested that this could have been a compensatory hypertrophy of an individual hamstring muscle, which could reasonably be expected to help offset deficits in mechanical stability. Taken together with the current results this suggests that hamstring muscle adaptations are individualistic and may be important in optimizing joint function for long-term joint health. The resultant regression equation can be interpreted from the current data as that for every ~ 15% less than the mean semitendinosus volume and every ~15% more than the mean biceps femoris long head volume there was a corresponding one degree larger LTS. It is of interest that there were no significant zero order correlations of LTS to muscle volumes. However when both semitendinosus and biceps femoris long head were accounted for, the zero order to semipartial correlations with LTS went from −0.20 to −0.62 and .21 to .59, respectively with both muscle volumes becoming significant predictors of LTS
Table 1 Descriptive data.
Lateral tibial slope (degrees) Semitendinosus volume (cm3)a Biceps femoris-long head volume (cm3)a a
Female
Male
Total
4.2 ± 1.6 151.4 ± 33.0 156.3 ± 27.6
4.4 ± 2.9 260.0 ± 64.5 247.3 ± 61.5
4.3 ± 2.4 203.1 ± 74.2 199.6 ± 65.2
Significant difference between sexes.
Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006
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Table 2 Stepwise regression results. Model
R
R2
R2 Δ
Sig. FΔ
1 2 3
.040 .356 .654
.002 .127 .428
.002 .125 .301
.862 .125 .008
Model 1 Predictors: (Constant), sex. Model 2 Predictors: (Constant), sex and semitendinosus volume. Model 3 Predictors: (Constant), sex, semitendinosus volume, biceps femoris long head volume.
in the final model. This demonstrates that the individual muscle volumes were uniquely associated with LTS only when accounting for the influence of the other. These findings highlight the antagonistic–agonistic relationship of the medial and lateral hamstrings in controlling internal tibial rotation. There is evidence to support that muscle function and skeletal geometry are related. It is well understood that muscles adapt to the load demands [35]. It is also commonly accepted that muscle forces can induce skeletal adaptation [36]. However, we were unable to locate any work investigating the direct adaptation of muscle to bony morphology. The current results suggest a potential that skeletal structure dictates long term loads and subsequent muscle morphology adapts to the requirements of these loads to mitigate loading of the passive restraints. In addition to the hamstrings as a group collectively resisting anterior tibial translation, the semitendinosus independently contributes to knee internal rotation moments whereas the biceps femoris independently contributes to external rotation moments [20]. Given that the ACL is strained to a greater extent during internal rotation compared to external rotation [9], it stands to reason that greater force producing capability of the biceps femoris associated with a greater volume of muscle would be needed to counteract the greater knee internal rotation moment created by a greater LTS during axial loading. Further, because of the bony predisposition to create knee internal rotation in those with greater LTS, there may be less overall demand placed upon the semitendinosus. This lesser demand would be associated with a decrease in strength and corresponding volume of the semitendinosus, while also acknowledging that neural drive actually controls force generation. Hamstring muscle strength training, with an emphasis on hypertrophic adaptation, has been suggested to reduce injury risk by correcting muscle size imbalances and the associated functional strength imbalances [33]. Specific to the greater risk of ACL injury associated with LTS, this would suggest that increasing the volume of the lateral hamstring may increase the ability to resist internal rotation or anterior translation of the tibia. Although both the medial and lateral hamstrings should be trained to resist anterior tibial translation, additional focus on the lateral hamstring may be of benefit to decrease ACL strain associated with a greater LTS and concomitant internal tibial rotation. Future research is needed to determine if supplemental hamstring strengthening exercises using variations in technique, which emphasize lateral hamstring efforts more than medial hamstring efforts, would better allow an individual to better resist internal tibial rotation and lessen the risk of ACL injury. The study was limited to the investigation of a single medial hamstring muscle and a single lateral hamstring muscle. Given the cost and difficulty of obtaining MRI data, the study was not statistically powered to examine the predictivity and inter-relationships of all four hamstring muscles. We chose not to combine the two medial and two lateral hamstrings to gain a better understanding of individual function. Individual hamstring muscle features such as muscle volume, moment arm length, pennation angle, physiological crosssectional area, and muscle fiber length differ across the hamstring muscles [20–22] and likely influence resultant joint moments. The semitendinosus and biceps femoris long head have different architectural arrangements with the biceps femoris better situated for force production having a high physiological cross sectional area whereas the semitendinosus is better suited for excursion with long fiber lengths relative to the muscle lengths [37]. Thus, there was rationale to look at their relationship to LTS in a non-summed manner. Also, the current study is limited by a lack of data on the relationships of tibial slope to muscle volume in an ACL-injured population. Prospective knowledge of muscle volume in those that subsequently sustain ACL injury would help to best determine the role of hamstring size in injury causation and direct future intervention efforts. Finally although hamstring volume has been previously correlated to measures of strength [32,33], the study did not assess direct measures of hamstring strength. 5. Conclusions Investigation of anatomic factors provides insight to a comprehensive prediction model for assessing injury risk. Healthy individuals with a greater posterior–inferior directed slope of lateral tibial plateau have relatively larger biceps femoris and smaller Table 3 Final regression model coefficients and correlations. Coefficients
Constant Sex (1F,2M) Semitendinosus volume Biceps femoris volume
Unstandardized beta
5.811 −.849 −.035 .034
Standardized beta
−.183 −1.091 .945
t
1.48 −.63 −3.27 2.99
Sig.
.157 .536 .005 .008
Correlations Zero-order
Partial
Semipartial
−.040 −.204 .209
−.151 −.621 .587
−.116 −.600 .549
Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006
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Lateral Tibial Slope (deg)
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Figure 3. 3D scatterplot of LTS, semitendinosus volume, and biceps femoris volume.
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Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006
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The Knee
Relationships of hamstring muscle volumes to lateral tibial slope☆ Randy J. Schmitz a,⁎, Anthony S. Kulas b, Sandra J. Shultz a, Justin P. Waxman e, Hsin-Min Wang c, Robert A. Kraft d a
The University of North Carolina at Greensboro, Greensboro, NC, United States East Carolina University, Greenville, NC, United States c China Medical University, Taichung, Taiwan d Wake Forest University, Winston-Salem, NC, United States e High Point University, High Point, NC United States b
a r t i c l e
i n f o
a b s t r a c t
Article history: Received 9 January 2017 Received in revised form 9 August 2017 Accepted 16 September 2017 Available online xxxx
Background: Greater posterior–inferior directed slope of the lateral tibial plateau (LTS) has been demonstrated to be a prospective ACL injury risk factor. Trainable measures to overcome a greater LTS need to be identified for optimizing injury prevention protocols.
Keywords: ACL injury Magnetic resonance imaging
Methods: Eleven healthy females (mean +/- standard deviation) (1.63 ± 0.07 m, 62.0 ± 8.9 kg, 22.6 ± 2.9 years) & 10 healthy males (1.80 ± 0.08 m, 82.3 ± 12.0 kg, 23.2 ± 3.4 years) underwent magnetic resonance imaging of the left knee and thigh. LTS, semitendinosus muscle volume, and biceps femoris long head muscle volume were obtained from imaging data.
It was hypothesized that Healthy individuals with greater LTS who have not sustained an ACL injury would have a larger lateral hamstring volume.
Results: After controlling for potential sex confounds (R2 = .00; P = .862), lesser semitendinosus volume and greater biceps femoris-long head volume were indicative of greater LTS (R2 Δ = .30, P = .008). Conclusions: Healthy individuals with greater LTS have a muscular morphologic profile that includes a larger biceps femoris-long head volume. This may be indicative of a biomechanical strategy that relies more heavily on force generation of the lateral hamstring and is less reliant on force generation of the medial hamstring. Level of evidence: Level IV. © 2017 Elsevier B.V. All rights reserved.
1. Introduction Biomechanical and neuromuscular factors have dominated the anterior cruciate ligament (ACL) injury risk-factor literature, as these risk factors seemingly have a relative ease of identification and potential for direct intervention and prevention. However, outcomes are mixed with regard to the effectiveness of screening movement biomechanics to predict injury risk [1–3]. A number of anatomical risk factors for ACL injury have been identified [4], but are often dismissed in prevention programming due to the perceived difficulty in modifying anatomical structure. As such, the development of interventions aimed to moderate injury risk in ☆ MRI data were obtained by support of the Gateway MRI Center at the University of North Carolina at Greensboro. ⁎ Corresponding author at: Dept. of Kinesiology, 256 Coleman, The University of North Carolina at Greensboro, Greensboro, NC 27402, United States. E-mail address: [email protected] (R.J. Schmitz).
https://doi.org/10.1016/j.knee.2017.09.006 0968-0160/© 2017 Elsevier B.V. All rights reserved.
Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006
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individuals with high-risk non-modifiable anatomical factors is of clinical importance for preventing knee injury and subsequent risk of early degenerative joint disease. The articular geometry of the knee is important in the transmission of joint loads and resultant movement biomechanics [5]. In this regard, posterior–inferior directed slope of lateral tibial plateau (LTS) has been increasingly studied as a potential risk factor [6]. A larger LTS has been associated with increasing ACL force during axial loading activities [7,8]. While both posterior medial and posterior lateral tibial plateau slopes can be obtained from magnetic resonance imaging (MRI) data, a larger LTS in combination with axial load is theorized to contribute to greater anterior tibial translation as well as greater internal tibial rotations [5], both of which are known to increase ACL strain [9]. Both retrospective [10] and prospective studies have identified a greater LTS as a risk factor for ACL injury [5] as well as a risk factor for re-injury to the ACL reconstructed knee [11]. While the structural nature of this risk factor cannot be easily modified, there is a need to consider ways that the surrounding musculature can be trained to either counteract or compensate for these structural variants. Thus, investigations of modifiable factors that may be related to such established anatomical risk factors are warranted. Given the agonistic relationship of the hamstrings to ACL function, available hamstring muscle volume (and subsequent force production capability) may be one means to counteract the mechanism by which LTS increases ACL strain and corresponding injury risk. Cadaver studies have demonstrated that the hamstrings' distal attachments on the proximal tibia and fibula allow this muscle group the ability to influence anterior–posterior displacement and internal–external rotation of the tibia relative to the femur [12– 15]. In addition, adequate co-contraction of the hamstrings has been shown to effectively reduce anterior translation and internal rotation of the tibia, thereby enhancing knee joint stability and reducing ACL strain [16–19]. As such, current ACL injury prevention and rehabilitation efforts often attempt to strengthen the hamstring muscle group as a whole in order to increase the net force applied by the hamstrings and thus enhance knee joint stability. However, given differential hamstring muscle function in the transverse plane [20], it may be of greater benefit to focus on the effects of individual hamstring muscle forces to reduce ACL loading. Although co-contraction of the hamstrings has been shown to effectively reduce anterior tibial displacement and internal tibial rotation [14,15], these findings have been established via symmetrical loading of the medial (i.e. semitendinosus and semimembranosus) and lateral hamstrings (i.e. biceps femoris short head and long head). Differences in morphological features that influence muscle force production such as muscle volume, pennation angle, physiological cross-sectional area, and muscle fiber length have been identified among different hamstring muscles [21,22]. In addition, it has been demonstrated that the lateral hamstring action is more influential on knee joint kinematics compared to medial hamstring action due a larger moment arm in the transverse plane [12,23]. It is possible that individuals with a steeper LTS may require a greater capacity for force production in the lateral hamstring musculature in order to better resist anterior tibial displacement and internal rotation. This in turn may protect the ACL from deleterious multi-planar loads. Thus the purpose of this study was to determine the relationship of individual medial and lateral hamstring muscle volumes to LTS. It was hypothesized that healthy individuals with greater LTS who have not sustained an ACL injury would have a larger lateral hamstring volume. Testing of the healthy individuals allows us to better determine muscular targets for future training/intervention work. 2. Materials and methods 2.1. Experimental protocol Eleven healthy females (mean +/- standard deviation) (1.63 ± 0.07 m, 62.0 ± 8.8 kg, 23.6 ± 2.7 years) and 10 healthy males (1.80 ± 0.08 m, 82.3 ± 12.0 kg, 23.5 ± 3.8 years) attended one session in which they underwent MRI examination. Healthy was defined as no current orthopedic injury or history of significant injury or surgery in left limb. Height, weight, and age were obtained along with an MRI assessment of muscle volume and tibial geometry. All measures were obtained on the left limb (preferred stance limb in 18/21 participants). MRI examination of the left limb was performed with a three tesla MRI system (Trio, Siemens, Erlangen, Germany) using a 15 channel transmit/receive high resolution knee coil and a combined spine and body coil for the hamstring muscle volume measures. Tibial geometry measurements were acquired with T1-weighted fat suppressed sagittal MRI scans of the tibiofemoral joint (Slice Thickness = 0.6 mm, In-Plane Resolution = 0.5 mm × 0.5 mm, Number of Slices = 176, FoV = 320 × 320 mm, TR = 1200 ms, TE = 33 ms, Flip Angle mode = PdVar, Bandwidth (Hz/pixel) = 539 Hz. Fat Suppression = SPAIR. Acquisition time = 8:29). Muscle volume measurements were obtained with T1-weighted fat suppressed frontal MRI scans of the thigh (Slice Thickness = 1.0 mm, In-Plane Resolution = 3.0 mm × 3.0 mm, Number of Slices = 256, FoV = 480 × 480 mm, TR = 1200 ms, TE = 33 ms, Flip Angle mode = PdVar, Bandwidth (Hz/pixel) = 539 Hz. Fat Suppression = SPAIR. Acquisition time = 8:29). The resulting images allowed visualization of both the hip joint and knee joint. 2.2. Tibial slope measurement Using MIPAV software (http://mipav.cit.nih.gov), LTS was measured by a single examiner as described by Hudek et al. [24]. First, the central sagittal image was selected on which the tibial attachment of the posterior cruciate ligament (PCL), the intercondylar eminence, and the anterior and posterior tibial cortices appeared in a concave shape. Next, two circles (proximal and distal) were drawn in the proximal tibia. The proximal circle touched the anterior, posterior, and superior tibial cortex bone and the distal circle had to touch the anterior and posterior cortex border. A standardized relative distance between the proximal and distal circles was established as the center of the distal circle was placed on proximal circle circumference Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006
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(Figure 1). The longitudinal axis of the tibia was then defined by a line connecting the centers of two circles and was transposed to all slices. The articulation center of the lateral tibial compartment was selected from an axial view, and a line was connected between the most anterior and posterior points of the lateral tibial plateau using the sagittal view. LTS was then defined by the angle formed by orthogonal to the MRI-longitudinal axis and the tangent to the lateral plateau (Figure 2). A posteriorly–inferiorly sloping value was defined as positive. The single LTS examiner established between-day intratester reliability and precision by reassessing 12 participants separated by at least 48 h (intraclass correlation coefficient +/- standard error of measurement) (ICC2,1 ± SEM = 0.98 ± 0.4°). 2.3. Muscle volume measurement For the medial hamstring, the semitendinosus was selected due to its slightly larger internal rotation moment arm [20]. For the lateral hamstring, the long head of the biceps femoris was selected for its larger external moment arm [20], and because it is more susceptible to injury and dysfunction than the semimembranosus [25]. Additionally, the biceps femoris long head produces more force than the short head during early stance [26], a time in weight acceptance commonly associated with noncontact ACL injury [27]. Further, reduced activity of this muscle has been predictive of ACL injury [28]. A single investigator calculated muscle volumes from serial anatomical cross-sectional areas (CSAs) of the semitendinosus and long head of the biceps femoris muscles in 2.25 cm intervals from the lateral knee joint line to the ischial tuberosity for each individual hamstring muscle in Osirix v5.7.1 (Osirix Foundation, Geneva Switzerland). Additional CSAs were measured at the most proximal and distal ends of each of the muscles where muscle tissue could be visualized. For each muscle, the CSAs were plotted against femur length and then fitted with a cubic spline. Volumes of the semitendinosus and long head of the biceps femoris were then calculated as the area under the CSA vs. femur length curves [29,30]. The investigator established betweenday intratester reliability and precision by re-measuring the muscle volumes of 10 participants separated by at least 48 h (ICC2,1 range ± SEM range) (0.99–0.99 ± 1.5–1.6 cm3). 2.4. Statistical analyses A linear regression was used to predict LTS. To control for reported sex differences in LTS [31], sex was initially entered on the first step. Semitendinosus volume and biceps femoris-long head volume were entered in a forward stepwise manner on subsequent steps. 3. Results Descriptive data are presented in Table 1. After controlling for sex (R2 = .00; P = .862), lesser semitendinosus volume and greater biceps femoris-long head volume predicted greater LTS (R2 Δ = .30, P = .008) (Table 2). Both muscles were significant predictors in the final model. Notably there were relative increases in magnitudes of the partial correlations relative to the zero order correlations of semitendinosus volume to LTS and biceps femoris volume to LTS (− 0.20 to − 0.62 and .21 to .59,
Figure 1. Central sagittal image with center proximal (0) and distal (1) circles defined. The proximal circle touched the anterior, posterior, and superior tibial cortices while the distal circle had to touch the anterior and posterior cortices. The line connecting these two centers was defined as the longitudinal axis of the tibia.
Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006
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Figure 2. Central sagittal image of lateral tibial plateau. Lateral tibial slope (LTS) was defined as the angle formed by a line orthogonal to the longitudinal axis and a line tangent to the lateral tibial plateau.
respectively) in the final model (Table 3). A scatterplot of muscle volumes and LTS is found in Figure 3. The resultant prediction equation was: LTS = 5.81 − .849Sex − 0.035semitendinosus volume + 0.034biceps femoris long head volume. 4. Discussion A better understanding of modifiable factors that have the potential to compensate for or counteract known anatomical risk factors for ACL injury may lead to more focused and effective injury prevention efforts. In this regard, we undertook a study that aimed to determine the relationship of individual medial and lateral hamstring muscle volumes to the established ACL risk factor of LTS. Because muscle volume is commonly understood to be modified through training interventions that induce muscle hypertrophy, we may be able to effectively reduce ACL loading and subsequent ACL injury risk by counteracting the biomechanical effects of LTS during axial loading. The following discussion addresses potential mechanisms of interaction between bony geometry and individual hamstring muscle function. The current results suggest an overarching idea that individual muscles may adapt to bony geometry as individuals with greater LTS have lesser semitendinosus muscle volume and larger biceps femoris muscle volume. Because hamstring volume has been previously correlated to measures of strength [32,33], we have reason to believe that the volume measures are related to strength capacity. This suggests that healthy individuals with a bony geometry that predisposes them to internal rotation during axial loading of the knee joint [5] may have a resultant biomechanical strategy that relies more heavily on force generation of the biceps femoris to control internal tibial rotation and is less reliant on force generation of the semitendinosus muscle. The concept of individual muscle adaptations to a stimulus is supported through previous literature. Although not related to joint bony geometry, individual hamstring muscles adapt following ACL surgery [34]. In a follow-up study of patients who underwent ACL reconstruction with a hamstring tendon graft at least two years previously, there was a 7.7% larger biceps femoris long head volume in the surgical limb compared to the contralateral limb [34]. The authors suggested that this could have been a compensatory hypertrophy of an individual hamstring muscle, which could reasonably be expected to help offset deficits in mechanical stability. Taken together with the current results this suggests that hamstring muscle adaptations are individualistic and may be important in optimizing joint function for long-term joint health. The resultant regression equation can be interpreted from the current data as that for every ~ 15% less than the mean semitendinosus volume and every ~15% more than the mean biceps femoris long head volume there was a corresponding one degree larger LTS. It is of interest that there were no significant zero order correlations of LTS to muscle volumes. However when both semitendinosus and biceps femoris long head were accounted for, the zero order to semipartial correlations with LTS went from −0.20 to −0.62 and .21 to .59, respectively with both muscle volumes becoming significant predictors of LTS
Table 1 Descriptive data.
Lateral tibial slope (degrees) Semitendinosus volume (cm3)a Biceps femoris-long head volume (cm3)a a
Female
Male
Total
4.2 ± 1.6 151.4 ± 33.0 156.3 ± 27.6
4.4 ± 2.9 260.0 ± 64.5 247.3 ± 61.5
4.3 ± 2.4 203.1 ± 74.2 199.6 ± 65.2
Significant difference between sexes.
Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006
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Table 2 Stepwise regression results. Model
R
R2
R2 Δ
Sig. FΔ
1 2 3
.040 .356 .654
.002 .127 .428
.002 .125 .301
.862 .125 .008
Model 1 Predictors: (Constant), sex. Model 2 Predictors: (Constant), sex and semitendinosus volume. Model 3 Predictors: (Constant), sex, semitendinosus volume, biceps femoris long head volume.
in the final model. This demonstrates that the individual muscle volumes were uniquely associated with LTS only when accounting for the influence of the other. These findings highlight the antagonistic–agonistic relationship of the medial and lateral hamstrings in controlling internal tibial rotation. There is evidence to support that muscle function and skeletal geometry are related. It is well understood that muscles adapt to the load demands [35]. It is also commonly accepted that muscle forces can induce skeletal adaptation [36]. However, we were unable to locate any work investigating the direct adaptation of muscle to bony morphology. The current results suggest a potential that skeletal structure dictates long term loads and subsequent muscle morphology adapts to the requirements of these loads to mitigate loading of the passive restraints. In addition to the hamstrings as a group collectively resisting anterior tibial translation, the semitendinosus independently contributes to knee internal rotation moments whereas the biceps femoris independently contributes to external rotation moments [20]. Given that the ACL is strained to a greater extent during internal rotation compared to external rotation [9], it stands to reason that greater force producing capability of the biceps femoris associated with a greater volume of muscle would be needed to counteract the greater knee internal rotation moment created by a greater LTS during axial loading. Further, because of the bony predisposition to create knee internal rotation in those with greater LTS, there may be less overall demand placed upon the semitendinosus. This lesser demand would be associated with a decrease in strength and corresponding volume of the semitendinosus, while also acknowledging that neural drive actually controls force generation. Hamstring muscle strength training, with an emphasis on hypertrophic adaptation, has been suggested to reduce injury risk by correcting muscle size imbalances and the associated functional strength imbalances [33]. Specific to the greater risk of ACL injury associated with LTS, this would suggest that increasing the volume of the lateral hamstring may increase the ability to resist internal rotation or anterior translation of the tibia. Although both the medial and lateral hamstrings should be trained to resist anterior tibial translation, additional focus on the lateral hamstring may be of benefit to decrease ACL strain associated with a greater LTS and concomitant internal tibial rotation. Future research is needed to determine if supplemental hamstring strengthening exercises using variations in technique, which emphasize lateral hamstring efforts more than medial hamstring efforts, would better allow an individual to better resist internal tibial rotation and lessen the risk of ACL injury. The study was limited to the investigation of a single medial hamstring muscle and a single lateral hamstring muscle. Given the cost and difficulty of obtaining MRI data, the study was not statistically powered to examine the predictivity and inter-relationships of all four hamstring muscles. We chose not to combine the two medial and two lateral hamstrings to gain a better understanding of individual function. Individual hamstring muscle features such as muscle volume, moment arm length, pennation angle, physiological crosssectional area, and muscle fiber length differ across the hamstring muscles [20–22] and likely influence resultant joint moments. The semitendinosus and biceps femoris long head have different architectural arrangements with the biceps femoris better situated for force production having a high physiological cross sectional area whereas the semitendinosus is better suited for excursion with long fiber lengths relative to the muscle lengths [37]. Thus, there was rationale to look at their relationship to LTS in a non-summed manner. Also, the current study is limited by a lack of data on the relationships of tibial slope to muscle volume in an ACL-injured population. Prospective knowledge of muscle volume in those that subsequently sustain ACL injury would help to best determine the role of hamstring size in injury causation and direct future intervention efforts. Finally although hamstring volume has been previously correlated to measures of strength [32,33], the study did not assess direct measures of hamstring strength. 5. Conclusions Investigation of anatomic factors provides insight to a comprehensive prediction model for assessing injury risk. Healthy individuals with a greater posterior–inferior directed slope of lateral tibial plateau have relatively larger biceps femoris and smaller Table 3 Final regression model coefficients and correlations. Coefficients
Constant Sex (1F,2M) Semitendinosus volume Biceps femoris volume
Unstandardized beta
5.811 −.849 −.035 .034
Standardized beta
−.183 −1.091 .945
t
1.48 −.63 −3.27 2.99
Sig.
.157 .536 .005 .008
Correlations Zero-order
Partial
Semipartial
−.040 −.204 .209
−.151 −.621 .587
−.116 −.600 .549
Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006
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Lateral Tibial Slope (deg)
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Figure 3. 3D scatterplot of LTS, semitendinosus volume, and biceps femoris volume.
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Please cite this article as: Schmitz RJ, et al, Relationships of hamstring muscle volumes to lateral tibial slope, Knee (2017), https:// doi.org/10.1016/j.knee.2017.09.006