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RESEARCH

Volume 8 Issue 1 | Spring 2015

The relationship between trunk muscle strength and flexibility, intervertebral disc wedging, and human lumbar lordosis Connie Hsu1, Eric Castillo2, and Daniel Lieberman3 1

Harvard College ‘16 Department of Human Evolutionary Biology, Harvard University 3 Department of Human Evolutionary Biology, Harvard University 2

Introduction

Functions of various trunk muscles Lumbar lordosis not only stabilizes the spine by maintaining sagittal balance of the upper body’s center of mass, but it also allows for greater sagittal flexion and extension of the trunk due to the orientation of lumbar zygapophyseal joints (Berlemann et al., 1999; Hildebrand, 1974; Guan et al., 2007). Agonist-antagonist muscle groups control sagittal movements of the trunk. The extensor muscles of the lower back, including the Multifidus muscle of the Transversospinalis group and the Erector Spinae muscles, provide mechanical stability and play an important role in controlling movement of the lumbar spine (Hansen et al., 2006; Macintosh & Bogduk, 1986). Other muscles in the lower back include the Psoas Major – which connects the transverse processes of lumbar vertebrae to the lesser trochanter of the femur and contributes to flexion of the trunk, and the Quadratus Lumborum – which primarily functions to brace the lower ribs and provide a steady base for thoracic muscle fibers. The Quadratus Lumborum may also assist in support and movement in lateral bending (Adams et al., 2006). The degree of lordosis in the lumbar spine induces the conversion of power - or a transfer of strength – developed in the back extensor muscles to transfer axial torsion forces, the twisting motion of a torque around

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Physiology

Human axial skeletons possess many derived adaptations for bipedalism, including a posteriorly concave curvature of the lumbar spine known as lordosis (Whitcome et al., 2007). Although humans are morphologically and genetically similar to the African great apes, chimpanzees and gorillas are knuckle-walking quadrupeds, lacking the lordotic curve derived in humans. This may partly be explained by variations in regional vertebral numbers between great apes and humans. Although the total number of vertebrae remains consistent, great apes possess fewer (three to four) lumbar vertebrae and an average of 13 thoracic vertebrae as opposed to an average of five lumbar and 12 thoracic vertebrae in humans. The greater number of lumbar vertebrae in humans likely contributes to the greater range of motion and curvature in human lower backs (Whitcome, 2012). Lumbar lordosis is essential for balancing the human body in an upright posture, and it develops early on in ontogeny when infants begin learning how to walk (Abitol, 1987). However, lordosis is not a uniquely human trait. For example, Japanese macque monkeys trained to walk bipedally also demonstrate a lumbar lordosis, suggesting that lordosis serves an important biomechanical function (Preuschoft et al., 1988). In addition to lumbar lordosis, the the range of motion of the spine differentiates human and non-human primate lower backs (Sparrey et al., 2014). The orientation of the vertebrae that shape the short, flat lumbar spines of great apes are less flexible than human spines, and offer very little mobility, suggesting that changes in lumbar curvature and range of motion were adaptive (Lovejoy, 2005). Indeed, the evolution of human lumbar lordosis required reorganization of the spinal musculature to support bipedal locomotion while maintaining stability and strength in the lower back (Lovejoy, 2005). The mobility of the lumbar spine is especially important because the lumbar region tends to experience the greatest weightbearing loads in the spine, and it is a common site of low-back pain (Battie et al., 2009). While it is unclear how lumbar mobility and lordosis contribute to low back pain, previous studies have discovered that both spinal muscle strength and intervertebral disc morphology are associated with the degree of lordotic curvature (Sinaki et al., 1996; Whitcomb et al., 2007; Sparrey et al., 2014). The aims of this study attempt to investigate whether strength of relative trunk muscles – specifically, the ratio of hypaxial (front) and epaxial (back) muscles – and degree of disc wedging , which is likely involved in stability and flexibility of the lower back, are associated with lumbar lordosis curvature.

Intervertebral disc morphology and flexibility of the lower spine The morphology of intervertebral discs affects the amount of lordosis and mobility of the lumbar region. Intervertebral discs separate adjacent vertebrae, allow for movement, and resist loading between vertebrae (Adams et al., 2006). Previous studies have indicated that loading of the spine significantly compresses the discs especially in the L4-5 and L5-S1 lumbar regions, which have greatest sagittal, or vertical, range of motion (Shymon et al., 2014). Compression and shearing of discs (See Figure 1 for descriptions) may be related to a higher risk of disc disease and instability in the lower spine (Shymon et al., 2014). Since intervertebral discs provide most of the spine’s intrinsic resistance to small movements (including compression, torsion, and shearing forces), discs are likely locations of instability. Conditions such as degenerative disc disease are correlated with reduced lordosis in the lumbar spine (Barrey et al., 2007), likely due to an inability of the diseased disc to allow for the same range of motion as a healthy disc. It is possible that certain morphological features of the disc, such as disc height, are associated with variations in flexibility of the lumbar spine, which may be crucial for determining rehabilitation methods for disc-related lower back pain targeted at particular disc levels for strengthening the back without sacrificing flexibility.

RESEARCH

Physiology

a vertical axis, that are necessary to rotate the pelvis while walking (Sparrey et al., 2014). The abdominal muscles in the trunk that are antagonistic to the back muscles include the Rectus Abdominus, Transversus Abdominus, Internal Abdominal Oblique, and External Abdominal Oblique. The Rectus Abdominus, the muscle commonly targeted in abdominal workouts, originates on the pubis and inserts on the xiphoid process of the sternum and the costal cartilages of the ribs and is responsible for flexion of the spine in the sagittal plane (See Figure 2 for a visual of the muscle groups). Trunk muscles and stability in the lower spine The strength of agonist-antagonist trunk muscles is important for postural stability. In general, the cross-sectional area of a muscle correlates with its strength because the capacity of a muscle to generate force is directly proportional to the number and size of the muscle fibers within it (Akagi et al., 2009, Blazevich et al., 2009). Mathematical modeling predicts that larger muscle forces are required for lumbar stability, which depends on the degree of lumbar curvature (Meakin & Aspden, 2012). This suggests a relationship between muscle size and sagittal lumbar curvature. Previous studies have indeed found that the volume of the lumbar extensor muscles (including the Multifidus and Erector Spinae muscles) are positively correlated with the magnitude of lordosis curvature in the lumbar regions, indicating that larger muscle forces are required for stabilization in populations with greater lumbar lordosis (Meakin et al., 2013). In addition, decreased trunk extensor muscle volume is correlated with back pain (Danneels et al., 2000; Kamaz et al., 2007). However, the relationship between strength of the antagonistic trunk flexor muscles, such as Rectus Abdominis, with flexibility and curvature of the lower back has not yet been thoroughly investigated.

Figure 1: Degree of lumbar lordosis and forces acting on the lower spine (Castillo et al., 2015). Shearing forces represent horizontal forces acting on the spine. Compression refers to perpendicular forces acting on the spine. Trunk weight refers to the vector sum of the weight-bearing forces acting on the spine.


Variation in lumbar lordosis vs. strength and flexibility There is a considerable range of variation in lumbar sagittal curvature in humans (Berthonnaud et al., 2005; Boulay et al., 2006), possibly due to factors such as change in posture or intrinsic bony anatomy (Meakin et al., 2012). Previous studies have shown this variability to be correlated with variation in back extensor size and strength (Danneels et al., 2000; Kamaz et al., 2007; Hides et al., 2008; Wallwork et al., 2009). Even though abdominal flexor muscles and back extensor muscles require coactivation in order to provide mechanical stability in the spine, the extent to which they are activated differs between individuals, implying that different individuals use different patterns of flexor or extensor muscle coactivation to stabilize the lumbar spine (Cholewicki et al., 1997), which may explain some variations in lumbar curvature. Little is known about how sagittal spinal range of motion relates to variations in lordosis and trunk stability. Previous interventions aimed at increasing spinal stabilization while maintaining flexibility and mobility in patients after surgery have been plagued by complications and failures, perhaps indicating evidence for a trade-off between flexibility and range of motion with stability and strength in the lumbar spine (Shymon et al., 2014). Variations in lumbar lordosis are hypothesized to be correlated with a tradeoff between trunk muscle strength and sagittal lumbar flexibility, since muscle strength functions to maintain stability and stiffness of structures, while flexibility increases range of motion in joints but is often associated with structural instability in the trunk. There is also evidence that improving core muscle balance may be an effective intervention in correcting posture problems in young subjects as a prevention measure for back pain, possibly due to increased stability, but the outcomes of such an intervention are unknown (Scannell & McGill, 2003). This study tests the hypothesis that there is an underlying tradeoff between strength of the Rectus Abdominus and back (Erector Spinae, Multifidus, Quadratus Lumborum, or Psoas) muscle strength, which leads to variations in lumbar lordosis. The study also tests the hypothesis that lumbar lordodsis is associated with decreased rostral (back) disc height. A sample of magnetic resonance image (MRI) scans from healthy, young adult volunteers were analyzed to investigate factors affecting lumbar lordosis variations. In contrast to previous studies that found an association between lumbar extensor muscle volume lumbar lordosis (Meakin et al., 2013), we hypothesize that lumbar lordosis will covary with the relative strength of agonistantagonist trunk muscle groups. Thus, we predict that subjects with larger, and thus stronger, Rectus Abdominis muscles relative to lumbar extensor muscles have decreased lumbar curvature in the lower back due to the antagonistic role of the Rectus Abdominis in lower back movement (flexion, instead of extension). We also expect that subjects with larger lumbar extensors relative to trunk flexors will show increased lumbar curvature. In addition to trunk strength, we also test the hypothesis that soft-tissue factors, such as increased posterior wedging of the vertebral discs (as indicated from the rostral (back) disc height relative to the max disc height of that level) will be positively associated with an increased lumbar curvature. Testing the hypothesized trade-off between hypaxial and epaxial trunk strength in the lordotic spine will lead to a better understanding of how stability and range of motion interact to moderate variations in lumbar lordosis, which has important implications for the intervention and prevention of biomechanical risk factors for back pain.

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RESEARCH 400mm, and 300mm respectively, with a resolution of 1.280 pixels per mm for a slice thickness of 7mm. Axial imaging involved a FLASH scan consisting of scans with a height, width, and depth of 218mm, 350mm, and 250mm respectively, with a resolution of 1.463 pixels per mm for a slice thickness of 5mm.

Figure 2: This image is a FLASH scan of an axial view of the spinal musculature just above the L4/L5 disc. This image was selected randomly in order to avoid bias. This study targeted the Rectus Abdominus (blue), Erector Spinae (green), Multifidus (purple), Quadratus Lumborum (red), and Psoas (orange) muscle groups.

Subject Recruitment and Consent Thirty-one subjects (n=15 females and 16 males) were recruited from the greater Boston area. Subjects were young adults (18-35 years old) in good health to minimize age-related degenerative changes in the spine, such as arthritis, disc degeneration, or other spinal pathology. Potential subjects were screened using a health questionnaire, and any subjects who reported a history of back pain or diagnosed spinal pathology were excluded. The Committee of Use of Human Subjects on Institutional Review Board at Harvard University approved this study, and all subjects gave their written informed consent. Data Acquisition Magnetic Resonance Imaging (MRI) data from subjects was collected, along with their age, height, and body mass. Scans were conducted at the Center for Brain Science Neuroimaging lab (at Harvard University) with a 3-Tesla Siemens Tim Trio MRI scanner. Subjects were scanned in the supine position with their legs laying flat during the scan. To minimize image artifact due to diaphragm movement, FLASH scans were implemented with the subject holding their breath for 30 seconds. These scans were used in the analysis of the lumbar spine from an axial view. A single-slice localizer scan was used for analyses of the spine in the mid-sagittal plane. The standard protocol of the MRI scans consisted of sagittal and axial T1-weighted images [repetition time/echo times of 8.6/4 ms and 7.4/4 ms respectively]. The sagittal imaging involved a localizer single-slice with height, width, and depth of 400mm,

Statistical Analysis Statistical analysis of the data was conducted using Microsoft Excel and R statistical software (version 0.98.501). A Shapiro-Wilk test (Shapiro & Wilk, 1965) was completed on each of the independent variables - ratio of Rectus Abdominus muscle over back extensor muscles and disc wedging – as well as the dependent variable (LA) in order to establish whether the data followed a normal distribution. Multiple partial regression models were implemented to determine associations between lordosis angle and the hypaxial / epaxial strength ratio (measured as the cross-sectional areas of Rectus Abdominus to various back muscles), accounting for the effects of age, height, and weight as additional covariates. The multiple regression models with the greatest significance between the hypaxial / epaxial strength ratios and lordosis angles were then normalized to z-scores. Sample size power tests were implemented to determine the ideal sample size for a multiple regression model given the strength of the effect sizes (multiple R2). Cohen’s f2 effect size

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Physiology

Materials and Methods

Image Analysis MRI images were analyzed using ImageJ software (National Institutes of Health). Each measurement on cross-sectional area of the trunk muscles, lordosis angle, and disc heights were completed three times and averaged to ensure intra-individual measurement reliability. Coefficients of variation for intra-individual consistency were calculated for each of three measurements for all of the measured variables. Intervertebral disc wedging was assessed from the mid-sagittal localizer scan. Disc and vertebral wedging were analyzed using the tracing feature of ImageJ by measuring the anterior and posterior disc heights for the T12 through L5 vertebrae, as well as the maximum disc height at the T12-S1 intervertebral levels. Posterior disc wedging at each level was found by dividing the height of the disc in the posterior position by the maximum height of the disc at that level in order to determine the disc shape asymmetry due to wedging from various forces. The same strategy was used to calculate the degree of anterior disc wedging. Vertebral body height measurements were also taken at the above levels using the sagittal scan view. Since the cross-sectional area of a muscle is proportional to the capacity of the muscle to generate force, muscle strength was approximated by measuring the cross-sectional areas of muscle groups in axial view using FLASH breath-hold scans. The muscle groups analyzed included the Multifidus, Erector Spinae, Psoas, Quadratus Lumborum, and Rectus Abdominus muscles. Cross sectional areas of these muscles were traced at the L3/L4 and L4/L5 spinal levels. The cross-sectional areas of the muscles were then corrected for the non-orthogonal orientation of the scan plane relative to the orientation of the muscle cross-section by multiplying the measured cross sectional area by the cosine of the degree of vertebral body tilt at that spinal level (plus 45 degrees to ensure that tilt angles were all positive). The degree of lordosis, analyzed at the mid-sagittal plan using the angle feature in ImageJ, was measured as Cobb’s angle (lordosis angle; LA), which is defined as the intersection of vectors drawn along the superior endplate of the L1 vertebrae and superior endplate of S1 (see Been, 2011).

RESEARCH was calculated and used to estimate statistical power. The desired statistical power level for this test was P = 0.80, and the probability level used in the calculation was p = 0.05.

Physiology

Results Summary statistics and intra-individual measurement errors for anthropometrics and muscle cross-sectional areas are reported in Table 1. Subjects had a mean lumbar curvature of 49.0 degrees with a standard deviation of 9.64. In all models, height was negatively associated with lordosis angle, while weight and age were both positively associated with lordosis angle. Models also suggest that the ratio of the cross-sectional area of the Rectus Abdominus muscle to the cross-sectional area of various back extensor muscles – as a proxy for relative core versus back muscle strength – was negatively associated with lordosis angle for some muscle groups at specific spinal levels after accounting for age, height, and weight (Table 3). The three statistical models with the most significant strength ratios are shown with standardized beta coefficients in Table 3. All independent and dependent variables in these three models passed the Shapiro-Wilk test for normality. Sample size power tests were calculated to be 39, 34, and 35 (See Table 3) for each of the statistical models. The relationship between the ratio of the Rectus Abdominus muscle to the multifidus muscle and lordotic curvature at the L5 level had a coefficient of -0.33 approaching conventional significance levels (p = 0.087). A significant negative association between the ratio of the Rectus Abdominus muscle to the erector spinae

Figure 3: Partial regression, or added-variable, plots of the relationship between lordosis angle and ratio of Rectus Abdominus to the Multifidus muscle along with all its covariates (weight, height, and age) at the L5 level. All variables are scaled in order to compare strengths of relationships. Ratio.L5.RA.M refers to the ratio of the Rectus Abdominus muscle to the Multifidus muscle at the L5 level. “| others” refers to the partial regression model accounting for all covariates in the model while depicting the relationship between the main coefficient tested and the dependent variable (scaled lordosis angle).


muscle at the L3/L4 level and lordosis angle was found (coefficient = -0.41; p = 0.04). Furthermore, there was a significant negative association between the ratio of the rectus abdominus muscle to the Quadratus Lumborum muscle at the L3/L4 level and lordosis angle (coefficient = -0.36; p = 0.05). Graphical representations of each of these three statistical models along with their covariates are shown in Figures 3, 4, and 5. Summaries of the mean (SD) of posterior and anterior disc wedging at the L5/S1, L4/L5, L3/L4, L2/L3, and L1/L2 levels can be found in Table 4. Posterior disc wedging was significantly associated with degree of lordosis at the L2/L3, L3/L4, and L4/L5 levels (p