SPINE Volume 34, Number 24, pp 2626 2633 2009, Lippincott Williams & Wilkins

Neck Muscle Load Distribution in Lateral, Frontal, and Rear-End Impacts

A Three-Dimensional Finite Element Analysis
Soa Hedenstierna, PhD,* Peter Halldin, PhD,* and Gunter P. Siegmund, PhD

Study Design. A nite element (FE) model of the human neck was used to study the distribution of neck muscle loads during multidirectional impacts. The computed load distributions were compared to experimental electromyography (EMG) recordings. Objective. To quantify passive muscle loads in nonactive cervical muscles during impacts of varying direction and energy, using a three-dimensional (3D) continuum FE muscle model. Summary of Background Data. Experimental and numerical studies have conrmed the importance of muscles in the impact response of the neck. Although EMG has been used to measure the relative activity levels in neck muscles during impact tests, this technique has not been able to measure all neck muscles and cannot directly quantify the force distribution between the muscles. A numerical model can give additional insight into muscle loading during impact. Methods. An FE model with solid element musculature was used to simulate frontal, lateral, and rear-end vehicle impacts at 4 peak accelerations. The peak cross-sectional forces, internal energies, and effective strains were calculated for each muscle and impact conguration. The computed load distribution was compared with experimental EMG data. Results. The load distribution in the cervical muscles varied with load direction. Peak sectional forces, internal energies, and strains increased in most muscles with increasing impact acceleration. The dominant muscles identied by the model for each direction were splenius capitis, levator scapulae, and sternocleidomastoid in lateral impacts, splenius capitis, and trapezoid in frontal impacts, and sternocleidomastoid, rectus capitis posterior minor, and hyoids in rear-end impacts. This corresponded with the most active muscles identied by EMG recordings, although within these muscles the distribution of forces and EMG levels were not the same. Conclusion. The passive muscle forces, strains, and energies computed using a continuum FE model of the cervical musculature distinguished between impact directions and peak accelerations, and on the basis of prior studies, isolated the most important muscles for each direction.

Key words: nite element model, cervical musculature, impact biomechanics, muscle load, EMG. Spine 2009; 34:2626 2633

From the *Division of Neuronic Engineering, School of Technology and Health, Royal Institute of Technology, Stockholm, Sweden; and MEA Forensic Engineers & Scientists Ltd, Richmond, BC, Canada. Acknowledgment date: November 2, 2008. Revision date: April 20, 2009. Acceptance date: April, 21, 2009. The manuscript submitted does not contain information about medical device(s)/drug(s). Institutional and Foundation funds were received in support of this work. One or more of the author(s) has/have received or will receive benets for personal or professional use from a commercial party related directly or indirectly to the subject of this manuscript: e.g., honoraria, gifts, consultancies, royalties, stocks, stock options, decision making position. Address correspondence and reprint requests to Soa Hedenstierna, PhD, Neuronik KTH, Alfred Nobels Alle 10, 141 52 Huddinge, Sweden; E-mail: soah@kth.se

Neck injuries due to car collisions are a common problem in the western world.1,2 In the prevention and treatment of neck injuries, it is important to understand the injury mechanisms of the cervical spine. During the last 10 years, the importance of the cervical musculature has been identied as both a supportive structure and a site for soft tissue injuries.3 The signicance of the musculature as a stabilizer during loading has been reported in experimental studies4 7 and numerical analyses.8 13 However, the loading mechanism and load distribution between the neck muscles remains unclear. This is of interest for an improved understanding of how the head and neck is protected by the musculature and what role muscle strain plays in impact-induced neck pain. The response and relative contribution of the cervical muscles has been studied experimentally in volunteers using electromyography (EMG). Although EMG and muscle force are not directly related, EMG amplitude has been used to infer relative muscle force under isometric voluntary contractions. For instance, Kumar et al14 found that the sternocleidomastoid muscle was the largest contributor in exion and anterolateral exion contractions whereas trapezius was the largest contributor in extension and splenius capitis was the largest contributor in lateral exion. Schu ldt and Harms-Ringdahl15 also used EMG to show that trapezius and cervical erector spinae made maximal contributions during voluntary extension, whereas splenius and levator scapulas did so during lateral exion. During the imposed neck motion that develops in a vehicle impact, the cervical muscles may be loaded differently than during voluntary motion. The experimental results have shown that muscle activation depends on load direction and peak impact acceleration.16 20 According to Kumar et al16 18 the main load bearer is sternocleidomastoid in rear-end impacts, trapezius in frontal impacts, and splenius capitis in lateral impacts. For rearend impacts Siegmund et al19 reported high EMG activity in the inferior sternohyoid and sternocleidomastoid muscles, as well as some supercial and deep posterior muscles during the early phase of head extension. One difculty with EMG is that it has not been possible to measure all cervical muscles. Surface electrodes capture signals from relatively larger volumes and give rise to crosstalk if electrode pairs are placed too closely. With wire elec-

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trodes it is possible to measure deeper muscles,19,21,22 but they record local signals that can potentially be specic to a single compartment within a muscle and still it is difcult to reach all muscles due to their location. Volunteer studies are also restricted with regard to the magnitude of the impact, since injury risk must be minimized. In contrast to EMG studies, numerical models can be used to study all cervical muscles simultaneously and can be subjected to any range of acceleration. Moreover, muscle load can be quantied directly using different measures (e.g., force, energy, and strain) depending on the aim of the analysis. One concern in muscle load analyses is the individual active muscle response. Large variations in activation schemes and the lack of activation data for some muscles increase the uncertainty of these analyses. One way to address this uncertainty is to exclude activation and to clarify the individual muscle loads using a purely passive response. This type of analysis will highlight the muscles best able to control the induced dynamics and should correspond closely with the muscles enlisted by the neuromuscular system in vivo. If so, passive numerical models could be an important complement to the experimental analyses of muscle mechanics. The objectives of this study were to quantify muscle loads in the nonactivated cervical musculature using a 3D continuum Finite Element muscle model, to analyze the relation between load and both impact direction and severity, and to compare the numerical model with experimental EMG results. Materials and Methods
The numerical model used in the study (Figure 1) represents a 50th percentile male and was developed at the Department of

Table 1. The Muscles Included in the KTH Muscle Model, With Mass and Length*
Muscles S S S S P P P P P P P P P P S S A A A A P A A A Rectus capitis posterior major Rectus capitis posterior minor Obliquus capitis superior Obliquus capitis inferior Semispinalis capitis Semispinalis cervicis Longissimus capitis Longissimus cervicis Iliocostalis cervicis Multidus Splenius capitis Splenius cervicis Levator scapula Trapezius (cervical part) Rectus capitis anterior Rectus capitis lateralis Longus colli Longus capitis Scalenus anterior Scalenus medius Scalenus posterior (not entire muscle) Sternocleidomastoid Sternohyoid/sternothyroid Suprahyoid Abbreviation RCapMaj RcapMin OblSup OblInf SsCap SsCerv LongCap LongCerv IlioCerv Mult SplCap SplCerv LevScap TZ RCapAnt RCapLat LongColli LongCap ScalAnt ScalMed ScalPost SCM SH SupHyoid Mass (g) 3.46 1.45 1.6 3.33 44.4 24.2 16.6 4.4 55 32.1 15.5 47.7 105.4 0.61 1.0 10.2 8.6 8.5 14.4 6.7 Length (mm) 61 33 51 51 285 200 237 150 440 260 290 160 252.5 33 29 188 115 115 139 84

49.2 229 15.2 105 Springs

*The letters P, A, and S denote if it is grouped as a posterior, anterior, or suboccipital muscle. The abbreviations for each muscle are used in subsequent gures, tables, and the text.

Neuronic Engineering, KTH,8,23,24 using LS-DYNA software.25 The model includes the cervical vertebrae, facet joints, cervical ligaments, intervertebral discs, a rigid skull, rigid shoulders, and an elastic torso. The ligamentous spine model has been validated both at the motion segment level and as an entire cervical spine.8 The newly developed solid element musculature includes nonlinear viscoelastic material properties (Ogden rubber) derived from experimental data26 and a 3D geometry on the basis of magnetic resonance images.24,27 The kinematics of the nal model have been compared against volunteer experiments with good correlation, in rear-end, frontal, and lateral impacts24 and includes 22 separate pairs of muscles with mass and length according to Table 1.

FE Simulations
The neck model was subjected to sinusoidal acceleration impulses with a duration of 100 milliseconds applied to the rst thoracic vertebra (T1). Three different impact directions (simulating rear-end, frontal, and lateral impacts) and 4 peak accelerations (1, 5, 10, and 15 g), reaching from very low to moderate/severe impacts, were studied (Table 2). T1 was constrained in all other displacements and all rotations. No muscle activation was included during the simulations.

Table 2. The 12 Simulations Performed With 3 Different Directions and 4 Peak Accelerations
1g Rear-end (x) Frontal (x) Lateral (y) 1R 1F 1L 5g 5R 5F 5L 10 g 10R 10F 10L 15 g 15R 15F 15L

Figure 1. The KTH neck model including the continuum element musculature.

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Table 3. The Muscles and Directions Included in the EMG Experimental Studies by Kumar et al16 18 and Siegmund et al19
Impact directions Kumar et al1618 Siegmund et al19 Muscles Kumar et al1618 Siegmund et al19 Peak acc 1.4 g Peak acc 1.55 g TZ TZ SCM SCM Frontal 10 subjects Frontal 5 subjects SplCap SplCap Rear-end 7 subjects Rear-end 5 subjects Lateral 20 subjects Lateral 5 subjects

SsCerv

SsCap

Multif

LevScap

Load Distribution Analysis

For each simulation, the peak values were determined for 3 different muscle load measurements: cross-sectional force (N), Green-Lagrange effective strain (%),28 and internal energy (J). Cross-sectional force represents the stabilizing force exerted on the neck by a muscle and was computed for each muscle at a section close to the superior insertions but below any branching of the muscle. Force was calculated as the sum of element stresses multiplied by element cross-sectional area.25 Muscle strain reects the load distribution within a muscle and has been related to muscle injury potential29 and thus the peak value of the Green-Lagrange effective strain for all elements within a muscle was used for further analysis. Elements near the muscle insertions were removed from the strain analysis because the material stiffness in these regions did not reect the increased percentage of tendinous tissue. Internal energy quanties how much energy is stored in each muscle and how the muscle dampens the forces in the neck. Internal energy includes the energy absorbed in the muscles by deformation and viscoelastic effects. To compare different areas of the neck, the muscles were divided into 3 groups, anterior, posterior, or suboccipital (rectus capitis anterior and lateralis), depending on their location relative to the spinal column (Table 1). The total muscle mass was divided as anterior, 22%; posterior, 75.5%; and suboccipital, 2.5%.

frontal and lateral data were processed the same way as the published rear impact data.19 All EMG data were rectied, averaged, and normalized against maximum voluntary contractions. To enable comparison between the different entities of EMG, strain, force, and energy, each unit was normalized by its maximum value.

Results The maximum head displacement increased with increasing impact severity (Figure 2). At higher impact acceleration the head motion was restricted by contact with the torso. Load Distribution Analysis The load distribution in the cervical muscles varied with both impact direction and peak acceleration, and a few muscles dominated the sectional forces for each direction (Figure 3). In lateral impacts the cross-sectional force was greatest in levator scapulae and sternocleidomastoid (SCM), and in frontal impacts the force was greatest in splenius capitis (SplCap) and trapezius (TZ). In rear-end impacts, SCM, rectus capitis posterior minor (RCapMin), and at higher collision accelerations SH were the dominant muscles. This corresponds well with the muscles described as important voluntary force producers by Kumar et al and by Schu ldt and Harms-Ringdahl, except that cervical erector spinae and TZ were grouped together in the latter study.14,15 Strain Analysis Of the 3 load parameters, strain varied least with muscle size. The highest strains were typically found at the insertion areas of the muscle and the time of maximum

Comparison of FE Model Muscle Load and Experimental EMG Recordings During Impact
Neck muscle EMG activity during impacts has been measured in human subjects.16 19 Kumar et al used surface electrodes over 3 muscles and studied 3 impact-directions (Table 3). Siegmund used wire electrodes and measured 8 supercial and deep muscles in frontal, lateral, and rear-end impacts, although only the rear-impact data have been published.19 For this study, the

Figure 2. Maximum head displacement during impact analysis for different peak accelerations.

FE Neck Muscle Load Analysis Hedenstierna et al 2629

Figure 3. Sectional forces in 3 directions and 4 accelerations; and main force producers in corresponding directions.14,15 Muscles with * were measured jointly as TZ/cervical erector spinae.15

strain generally occurred when the head reached maximum displacement, except for the rear-end impact where the suboccipital muscle strains peaked during the head retraction before maximum extension. Strains were highest in lateral impacts and lowest in rear-end impacts (Figure 4). During lateral impacts high strains were seen in LevScap, SCM, TZ, and the Scalenus. During frontal impacts, high strains occurred in the extensor muscles, whereas for rear-end impacts high strains were found in the hyoid and suboccipital muscles. Strain generally increased with peak acceleration and in many cases increased almost linearly with T1 acceleration. Between 1 and 5 g, however, there was a clear change in strain distribution between muscles in all load directions. In rear-end impacts the strain increased rapidly and the highest values shifted from deep to supercial muscles. In frontal impacts the strain in the suboccipital muscles even decreased between 1 and 5 g.

Internal Energy Analysis The internal energy (Figure 5) increased with applied peak acceleration for all muscles except between 1 and 5 g, where it decreased for a few of the suboccipital muscles (RCapMin, OblSup, RCapAnt, and RCapLat). The sum of muscle internal energy (Table 4) was highest during frontal and lowest in rear-end impacts. As a percentage of the whole neck internal energy, rear-end impacts generated the lowest muscle energy. Internal energy increased with increasing peak T1 acceleration, especially between 1 and 5 g. Nevertheless, in relation to the total internal energy, the proportion of internal energy in the muscles decreased with increasing acceleration for all impact directions. In Figure 6, the muscles were divided into 3 groups and the energy in each group normalized by the total, so that the sum of all muscles equaled 1. When grouped into anterior, posterior, and suboccipital muscles, most of the

Figure 4. The peak effective green strain for each muscle during impacts of 1, 5, 10, and 15 g in lateral, frontal, and rearend impact simulations.

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Figure 5. Peak internal energy for each muscle during frontal impacts with increasing accelerations from 1 to 15 g. At the top left the maximum head displacement in m is plotted.

energy was absorbed in the posterior muscles and the least energy in the suboccipital muscles. For the 1 g rearend impact, the suboccipital muscles absorb almost 20% of the total muscle energy though they makeup only 2.5% of the total muscle volume. Comparison of Muscle Load Distribution and EMG During Impact The EMG data from the experimental studies differed but showed similar tendencies between muscles except for TZ in frontal impacts (Figure 7). The muscle loads predicted by the model for 1 g, did not correlate very well with the EMG data. The strain and energy was high in TZ and low in semispinalis cervicis compared to the normalized EMG levels. However, the muscles with the highest EMG values predicted high muscle loads and similar trends in load patterns could be seen. The strain distribution is similar to Siegmund EMG in lateral impact, except for LevScap and TZ; and in frontal impact Table 4. The Max Total Neck Muscle Internal Energy in Joule (J), and as Percentage of Total Neck Internal Energy, for the Different Directions and Peak Accelerations
Lateral % of Total 0.66 0.59 0.43 0.30 Frontal % of Total 0.63 0.57 0.47 0.39 Rear-End % of Total 0.58 0.45 0.28 0.21

except the TZ. The Kumar EMG was closer to the sectional forces in lateral and rear-end impacts. Discussion The present study has shown that passive muscle force, strain, and internal energy can be analyzed during impact loading using a 3D FE model of the cervical musculature. All measurements distinguished between impact directions and peak accelerations, and on the basis of previous studies, isolated the most important muscles for each impact direction. The muscles with highest EMG

Muscles 1g 5g 10 g 15 g 1.1 7.9 20.1 27.0

Muscles 1.5 10.0 21.0 29.8

Muscles 0.2 5.8 13.6 20.5

Figure 6. Muscle internal energy in posterior, anterior and suboccipital muscles during impact. The energy is normalized so that the total energy in all muscles equals one.

FE Neck Muscle Load Analysis Hedenstierna et al 2631

Figure 7. Normalized EMG data from impact loading experiments by Kumar et al16 18 and Siegmund et al19 together with 3 different load measurements from 1 g FE simulations.

recordings during impact also exhibited the highest muscle load parameters in the simulations. The current model has been validated for the material response in a single muscle27 and the kinematic responses of head and vertebrae during impact.24 Because of the complexity of the human neck, the model is necessarily a simplication of the human neck muscle system. The primary limitations of the model concern its material properties, the geometry of the tendinous insertions, and the boundary conditions between surrounding tissues.24,27 Despite these limitations, the complexity of the current model was considered sufcient to study the load distribution between muscles during various impact conditions. Since the myotendinous junctions at the insertions are a potentially important area for injury analysis,30 these could be improved in the model to give greater insight into explicit muscle injury mechanisms. Further, as the muscles with highest sectional force in this study corresponded to the muscles with proposed highest strength in the counteracting direction according to experimental studies (Figure 3), it was assumed that the model predicts a fairly accurate load distribution. Another simplication of the current study was the absence of muscle activation. As a rst step, we avoided the inclusion of active forces due to uncertainties related to the activation schemes. Future work, however, will need to incorporate muscle activations and assess how they alter the muscle load distribution. Load Measurements The distribution between muscles was different for the 3 computed variables, though they showed similar variations with impact direction and acceleration. The strain results were rened during postprocessing by removing insertion areas. A few elements were also discarded due to penetration in the contact interfaces between muscles. This occurred locally at the edge of some muscles and did not affect the kinematics. Though, this procedure im-

proved the reasonability of the strain results, it made them more subjective. In contrast, the energy included the entire muscle and the forces considered the predened cross section. The FE model predicts muscle strains that exceed the suggested failure strains of muscle (25% 60%)31,32 even at the 5 g level. This may be related to the lack of muscle activation and to the xed boundary condition of T1. In any case it highlights the need for more data on muscle mechanics during impact to validate a detailed muscle model. Impact Direction and Peak Acceleration The difference in muscle load distributions is clearly seen between 1 and 5 g while for accelerations above 5 g the loads are increasing almost linearly in some muscles. The change in load distribution for increased impact accelerations is mainly due to larger head kinematics. At low impact accelerations, a large part of the motion takes place between the skull and the rst cervical vertebra, resulting in relatively high loads in the suboccipital muscles. At higher impact accelerations, the head moves further and rotates so that the supercial and larger muscles take the main load at maximum head displacement. In rear-end impacts the model predicts, as expected from the literature,33 an S-shaped cervical column in the initial phase of the impact, with exion in the upper cervical spine and extension in the lower cervical spine. This results in high initial strains in the suboccipital muscles representing a high percentage of the total muscle energy (Figure 6). Muscle Load and Neck Injuries Neck injuries occur in all directions of impact, though the risk is higher in rear-end impacts.2 The energy absorbed by the muscles was highest during frontal impacts. In rear-end impacts, the absorbed energy and muscle strain was comparatively small (Table 4 and Figure

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4). This could mean that the ligamentous spine bears a larger part of the load during rear-end impacts, and therefore, could be injured at lower peak accelerations and speed changes than during frontal impacts. Further, the difference seen in load distribution between low and moderate/high accelerations, as well as the difference in the time of peak load between suboccipital and supercial muscles, could affect our ability to protect the cervical spine by muscle activation. FE Muscle Load and Experimental EMG Recordings The most common method used in neck muscle analysis today is EMG. Muscle activity (EMG) is not only a function of the applied external forces, but also of anticipation levels and cognitive cues such as sudden loud sounds.34 This means that the activity does not correspond solely to the actual physical load and is therefore problematic to use in comparison with muscle strain (Figure 7). Another uncertainty in EMG is the dependency on normalization and the ability to generate true maximum voluntary contractions. Because there is a redundant system of cervical muscles and a limited number of measured directions, it may not be possible to voluntarily evoke maximal contractions in each muscle. This may also explain why it is difcult to compare results from the experimental studies16 19 with different experimental protocols and different electrodes. In conclusion, there is a great need for more experimental data, both for input to numerical models and to increase the understanding of the muscular functions during impact loading. An interesting measurement for future study could be a combination of muscle strain and activation (EMG), because the usual failure mechanism of muscle is an eccentric contraction.29,35 Conclusion Using a continuum FE model of the cervical musculature exposed to 4 levels of impact severity in 3 directions, this study has shown that muscle force, strain, and energy generally increase with increasing acceleration. Moreover, we have shown that different muscles contribute to resisting the impact-induced motion under different impact directions (SplCap, LevScap, and SCM in lateral; SplCap and TZ in frontal; SCM, RcapMin, and SH in rear-end) and impact severities (a larger part of the load in the supercial muscles at high accelerations). Key Points

The model predicted that load distribution is dependent on impact direction and impact severity. The muscle loads did not have the same distribution between muscles as the experimental EMG data though the muscles with peak EMG recording during impact also predicted high muscle loads.

Acknowledgment The authors thank Jean-Se bastien Blouin of UBC School of Human Kinetics for his assistance with the EMG data. References
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An FE neck model with passive continuum musculature was used to identify important muscles in impacts from different directions. The model showed that the loads in most muscles increase with increasing impact energy.

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21. Gabriel DA, Matsumoto JY, Davis DH, et al. Multidirectional neck strength and electromyographic activity for normal controls. Clin Biomech 2004;19: 653 8. 22. Magnusson ML, Pope MH, Hasselquist L, et al. Cervical electromyographic activity during low-speed rear impact. Eur Spine J 1999;8:118 25. 23. Halldin P. Prevention and Prediction of Head and Neck Injury in Trafc AccidentsUsing Experimental and Numerical Methods [PhD-thesis at Department of Aeronautics]. Stockholm, Sweden: Royal Institute of Technology, KTH; 2001. 24. Hedenstierna S, Halldin P. How does a three-dimensional continuum muscle model affect the kinematics and muscle strains of a nite element neck model compared to a discrete muscle model in rear-end, frontal, and lateral impacts. Spine 2008;33:E236 45. 25. Hallquist JO. LS-DYNA Keyword Users Manual. Livermore, CA: Livermore Software Technology Corporation; 2007. 26. Myers BS, Van Ee CA, Camacho DL, et al. On the structural and material properties of mammalian skeletal muscle and its relevance to human cervical impact dynamics. In: Stapp Car Crash Conference Proceedings; 1995. 27. Hedenstierna S, Halldin P, Brolin K. Evaluation of a combination of continuum and truss nite elements in a model of passive and active muscle tissue. Comput Methods Biomech Biomed Engin 2008;11:62739. 28. Holzapfel GA. Nonlinear Solid Mechanics: A Continuum Approach for Engineering. Chichester, WS, United Kingdom: John Wiley; 2000. 29. Lieber RL, Friden J. Muscle damage is not a function of muscle force but active muscle strain. J Appl Physiol 1993;74:520 6. 30. Garrett WE Jr, Safran MR, Seaber AV, et al. Biomechanical comparison of stimulated and nonstimulated skeletal muscle pulled to failure. Am J Sports Med 1987;15:448 54. 31. Best TM. A Biomechanical Study of Skeletal Muscle Strain Injuries. Durham, NC: Department of Biomedical Engineering, Duke University; 1993. 32. Davis J, Kaufman KR, Lieber RL. Correlation between active and passive isometric force and intramuscular pressure in the isolated rabbit tibialis anterior muscle. J Biomech 2003;36:50512. 33. Ono K, Inami S, Kaneoka K, et al. relationship between spine deformation and cervical vertebral motions for low speed rear impacts using human volunteers. In: IRCOBI conference Sitges; 1999; Spain. 34. Siegmund GP, Inglis JT, Sanderson DJ. Startle response of human neck muscles sculpted by readiness to perform ballistic head movements. J Physiol 2001;535:289 300. 35. McCully KK, Faulkner JA. Injury to skeletal muscle bers of mice following lengthening contractions. J Appl Physiol 1985;59:119 26.