The Effect of Abdominal Stabilization Contractions on Posteroanterior Spinal Stiffness

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1 The Effect of Abdominal Stabilization Contractions on Posteroanterior Spinal Stiffness SPINE Volume 33, Number 6, pp , Lippincott Williams & Wilkins Tasha Stanton, BSc, PT, MScRS,* and Greg Kawchuk, DC, PhD* Study Design. Intrasubject controls with randomized intervention order. Objective. To quantify the immediate change in posteroanterior (PA) spinal stiffness produced by different combinations of trunk muscle contraction. Summary of Background Data. The abdominal hollow and the abdominal brace are 2 different combinations of trunk muscle contractions that are commonly prescribed to increase spinal stability. Unfortunately, the immediate effect of these different contractions on spinal stiffness (one indicator of spinal stability) has not yet been quantified directly. Methods. Twenty-eight asymptomatic subjects were taught abdominal hollow and brace contractions then performed them in a randomized order framed by periods of rest. Surface electromyography and B-mode ultrasound confirmed that all contractions were performed appropriately. During each test condition (hollow, brace, and rest), a noninvasive indentation technique was used to quantify PA spinal stiffness. A repeated measures analysis of variance was used to assess the significance of changes in the PA spinal stiffness between test conditions. Results. Both the abdominal hollow and abdominal brace contractions increased PA spinal stiffness significantly when compared with the rest condition (P 0.001). When the abdominal hollow and brace contractions were compared with each other, the abdominal brace contraction produced significantly greater PA spinal stiffness (P 0.05). Conclusion. In asymptomatic subjects, the abdominal brace contraction provided an immediate PA stiffening effect that was significantly greater in magnitude when compared with conditions of rest and abdominal hollowing. These findings may allow clinicians to better match commonly prescribed contraction-based interventions with specific patient needs. Future work is required to assess the long-term effect of repeated abdominal brace and hollow contractions on PA spinal stiffness and low back pain. From the *University of Alberta, Edmonton, Alberta, Canada; and University of Sydney, Sydney, NSW, Australia. Acknowledgment date: July 9, Revision date: September 19, Acceptance date: October 1, The manuscript submitted does not contain information about medical device(s)/drug(s). Federal, Institutional, and Foundation funds were received in support of this work. No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript. Support for this project and for Tasha Stanton was provided by the Province of Alberta Graduate Scholarship, the Strathcona Physiotherapy Foundation and NSERC. Support for Greg Kawchuk was provided by the Canada Research Chairs program. This study was approved by the University of Alberta Health Research Ethics Board. Address correspondence and reprint requests to Greg Kawchuk, 3-44 Corbett Hall, University of Alberta, Edmonton, Alberta, Canada T6G 2G4; greg.kawchuk@ualberta.ca Key words: stabilization, muscle contractions, posteroanterior spinal stiffness, abdominal hollow contraction, abdominal brace contraction. Spine 2008;33: Given its excessive financial and health burdens there is a tremendous need to understand the origins of low back pain (LBP), and the mechanisms by which various treatments may (or may not) convey their effect. Included in these treatments are various combinations of trunk muscle contractions thought to increase spine stability in the short and long term. As spinal function requires control of spinal movements and loads, 5 these contraction activities are often prescribed to address perceived problems in the muscular system s capacity to provide static and dynamic stabilization to the spine. Most commonly, these prescribed contractions include the abdominal hollow and/or the abdominal brace. The abdominal hollow contraction is performed by drawing in the lower abdomen while maintaining relaxation of the other abdominal muscles such as rectus abdominis and the obliques as well as contracting the small lower back muscles (close to the spine) while keeping larger back muscles relaxed. 6 These actions have been shown to activate transversus abdominis (TrA; a deep abdominal muscle) and multifidus (a deep lumbar spine muscle), respectively. 7 Preferential activation of these muscles is thought to provide intersegmental stability to the low back through an increase in intra-abdominal pressure and tensioning of the thoracolumbar fascia facilitated by TrA contraction 8,9 and direct control of intersegmental movement due to the unique intervertebral attachments of multifidus. 10 Because these effects have been theorized to help decrease low back pain, 5 prescription of the abdominal hollow stabilization contraction has been employed as a strategy to reduce LBP. 11,12 Further support for its prescription is given by observations in some LBP patients that TrA activity is altered and that the multifidus undergoes atrophy. 17 The abdominal brace contraction does not focus on specific muscle recruitment, rather, it involves global contraction of all abdominal and low back musculature. 18 This contraction is performed by tensing the entire trunk, without drawing in or pushing out 18 to create a generalized contraction of both the abdominal and back musculature. 7,18 20 Global activation of the trunk muscles is theorized to provide increased stability in all directions and in various types of movement which is thought to help minimize low back pain. 18,21 To date, we are unaware of any study that has monitored LBP in subjects who are prescribed this contraction. 694

2 Effect of Abdominal Stabilization Contractions on PA Spinal Stiffness Stanton and Kawchuk 695 Table 1. Exclusion Criteria Injury Related Disease Processes Subject Factors Current low back Osteoporosis pain Low back pain within Osteoarthritis the last year Previous back Rheumatoid surgery arthritis Lower extremity injury within the last year Ankylosing Spondylitis Known malignancy Known spondylolisthesis Multiple sclerosis Severe scoliosis Pregnancy (unsure or confirmed) Medications affecting muscle function (e.g., steroids) Medications affecting pain recognition (e.g., pain medications) Unable to tolerate indentation Unable to perform stabilizing exercises Although several studies have investigated the theoretical basis of these 2 contractions (e.g., which muscles are activated), very little clinical research has been performed to compare the presumptive effect of these 2 contractions: increasing spinal stability. Although Richardson et al found the abdominal hollow contraction to be more effective at increasing immediate stability, this study assessed the effect of these contractions in the sacroiliac joint. 7 Other studies that reported increased spinal stability with the abdominal brace contraction employed computational modeling, not direct measurement in humans. 19,20 Given the indirect approach of these studies toward assessing the effect of these contractions, as well as their conflicting results, there is a need to directly measure the effect of these 2 contractions on human lumbar spine stability. Therefore, the goal of this study was to quantify the immediate effect of 2 clinically distinct contractions on one indicator of spinal stability: posteroanterior (PA) spinal stiffness. It was hypothesized that both the abdominal hollow and abdominal brace contractions would increase PA stiffness of the spine compared with rest while the abdominal hollow contraction would increase PA stiffness to a greater extent than the abdominal brace contraction. Materials and Methods Subjects A total of 28 asymptomatic subjects between the ages of 18 to 50 were recruited to participate in this study (14 men and 14 women). This number was based on a priori calculations using a power of 80%, an expected mean difference of 17% 7 and a significance level of Potential subjects were excluded from this study primarily because of back pain and/or medical conditions that could affect subject safety during measurement of spinal stiffness (Table 1). 22 Written informed consent was obtained from all subjects before testing. This study was approved by the University of Alberta Health Research Ethics Board. General Protocol Training Session. Each subject was taught the abdominal hollowing contraction 6 and the abdominal brace contraction 18 by a single instructor using previously established teaching methodologies. To help prone subjects differentiate between the 2 stabilizing contractions, B-mode ultrasound and surface electromyography were used concurrently to determine the activation of both the deep and superficial trunk muscles. For the abdominal hollow, selective recruitment of TrA with minimal to no EMG activity of the superficial muscle groups was required to meet proper contraction performance. For the abdominal brace, increased EMG activity of the superficial muscles was required to meet proper contraction performance. If subjects were unable to selectively perform the 2 stabilizing contractions independently, they were dismissed from the study. Each contraction was described to the subjects with emphasis on a low force of contraction [10% 30% maximal voluntary contraction (MVC)]. 6 Testing Session. Subjects were asked to lie in the prone position while PA spinal stiffness was measured at the L4 vertebral level. Five familiarization events of simultaneous contraction and indentation were then performed. 23,24 With randomization of contraction events (i.e., hollow or brace), 10 indentations were performed during each of the following test conditions: rest, contraction, rest, contraction (Figure 1). Realtime B-mode ultrasound of the TrA (before and during contraction) and semg of the superficial trunk muscles were recorded concurrently during each indentation trial. A standard rest period of 2 minutes in the prone position was used between each indentation to ensure that the subject relaxed fully between measurements. PA Spinal Stiffness Assessment A more detailed description of the equipment used for indentation testing has been published previously. 25 In brief, an indentation device is used to apply an increasing PA indentation load to the external structures of the spine. A load cell and displacement transducer incorporated into the indenter allow measurement of the bulk tissue response to a given load (Figure 2). From these data, stiffness values can be calculated, which has been shown to have excellent accuracy 25 and reliability. 25a Indentation testing was performed by a single operator (T.S.) with over 150 hours of direct experience in this technique. In each prone subject, the L4 spinous process was identified by palpation. 26 The indentation device was then placed perpendicular to the L4 spinous process and advanced manu- Figure 1. Testing protocol involving 3 conditions: rest, abdominal hollow, and abdominal brace. A stiffness measurement was first taken at rest and then subjects were randomized to testing sequence 1 or 2. All subjects completed both sequences, differing only by the order in which the sequences were performed. A final measurement was taken at rest after completion of sequences. EMG and ultrasound were also measured during these same time periods.

3 696 Spine Volume 33 Number Figure 2. Assisted indentor. ally (approximately 2 mm/s) while subjects maintained a breath-hold at end-expiratory volume. 27 When a 100 N load was reached, loading was maintained for 1 second and then the indentation load was removed. From the resulting measures of applied load and indenter displacement, the PA spinal stiffness was quantified as 2 different outcome measures: (1) global stiffness (GS; slope of the force-displacement curve between 30 N and maximal force); and (2) mean maximal stiffness (MMS; average stiffness value in N/mm taken during the time period in which maximal indentation force has been delivered and held). Quality Control of Hollow and Brace Contractions Tranversus Abdominus Imaging During Contraction. Ultrasound imaging was performed using a Sonoline Sienna Siemens B-mode ultrasound (Siemens Medical Systems, Inc.; Issaquah, WA) with a 7.5-mHz linear array transducer. For each subject, the gelled ultrasound transducer was positioned 25 mm posteromedial to the midpoint between the ribs and ilium on the midaxillary line and parallel to the muscle fibers of TrA so that a hyperechoic interface between TrA and the thoracolumbar

4 Effect of Abdominal Stabilization Contractions on PA Spinal Stiffness Stanton and Kawchuk 697 Table 2. Subject Demographic Characteristics Mean SD Range Male Age (yr) Weight (kg) Height (m) BMI (kg/m 2 ) Female Age (yr) Weight (kg) Height (m) BMI (kg/m 2 ) maximal isometric trunk motions were then performed in the following order: flexion, right and left trunk rotation. 34 For the extensor muscles, a resisted maximal extension was performed with subjects in the prone position. 35 During the experiment, real-time EMG signals were employed to ensure the presence and/or absence of specific muscle activity. Figure 3. Adobe Photoshop image of the cross-sectional area of TrA (white) during a hollow contraction. fascia was visualized in the far right side of the ultrasound image. 28 Image gain, image focus, and the angle of the transducer were then adjusted to optimize visualization of the image. 28 During the experiment, real-time images were obtained in the above manner to ensure the presence and/or absence or TrA contraction. Image Analysis. A foot pedal switch that also synchronized EMG recordings was used to trigger ultrasonic image acquisition ( pixels) directly to an image capture board (National Instruments; Austin, TX). Offline, the muscular border of TrA was outlined from this image from its posterolateral fascial insertion to a specified distance into the muscle bulk of TrA and this distance measured using Abode Photoshop 7.0 (Adobe Systems, Inc.). The resulting distance was standardized within each patient and represented the smallest linear distance from the fascial insertion of TrA into the muscle belly of TrA (parallel to the fascial border of TrA). Image J 29 was then used to compute the cross-sectional area of each outlined TrA image. All cross-sectional area measurements were between muscle-fascia boundaries (Figure 3). 30 Reliability and validity evidence have been established for this method of measurement for TrA (Stanton and Kawchuk; submitted) and for the multifidus muscle. 31 EMG Collection. Each subjects skin was shaved over the EMG sites and cleaned with an alcohol swab. 32 Ag/AgCl bipolar disposable electrodes (Bortec BiPole) with an active diameter of 1 cm were then placed on the skin at 5 sites using an interelectrode distance of approximately 2 cm. Using a reference electrode placed over the clavicle, 5 channels of EMG were collected from the right side of the trunk (Bortec Biomedical; Calgary, Canada): rectus abdominis (3 cm lateral to the umbilicus), external oblique (approximately 15 cm lateral to the umbilicus), internal oblique (approximately midway between the anterior superior iliac spine and symphysis pubis, above the inguinal ligament), thoracic erector spinae (5 cm lateral to T9 spinous process), and lumbar erector spinae (3 cm lateral to L3 spinous process). 33,34 MVCs were then performed by subjects to normalize EMG magnitude. Specifically, for the abdominal muscles, each subject was situated in a sit-up position. Resisted Analysis of EMG Signals. The raw semg signals were A/D converted (16-bit), full wave rectified and low pass filtered with a second order single pass Butterworth filter. 34 A cutoff frequency of 2.5 Hz was used. 36 Using customized LABview software (National Instruments; Austin, TX), the average EMG amplitude over 1000 milliseconds was computed at the trigger points where ultrasound images were collected in time. The processed EMG data were then normalized to MVC amplitudes. Statistical Analysis. For data analysis purposes, data from all 5 of the familiarization events and the first experimental indentation in each test condition were discarded due to their known variability 23,24,37,38 A repeated measures analysis of variance of PA stiffness, EMG, and ultrasound data were performed to determine if significant differences occurred during the rest, hollow, and brace conditions. Results Demographics for the study population are shown in Table 2. An analysis of superficial muscle activity and TrA activity indicated that 3 distinct conditions occurred in our protocol (rest, abdominal hollow, and abdominal brace). As expected, superficial muscle activity and TrA activity were each silent during the prone rest condition. During the abdominal hollow contraction, significantly more TrA activity was present when compared with rest (Figure 4, P 0.001) with minimal superficial muscle activity. For the abdominal brace contraction, significantly more superficial muscle activity was present when compared with the abdominal hollow (Figure 5, P 0.001). Table 3 displays a comparison of expected versus observed EMG and TrA findings for each experimental condition. PA stiffness values for all individuals and trials are given in Table 4. Analysis of PA stiffness data revealed that both GS and MMS outcome measures increased as a result of the abdominal hollow and the abdominal brace contraction (Table 4, P 0.00). With application of the abdominal hollow, GS values increased, on average, 21.4% ( 23.2%) from rest while MMS values increased 26.8% ( 25.2%).

5 698 Spine Volume 33 Number Figure 4. Cross-sectional area of TrA during the rest, hollow, and brace conditions. Difference values represent the difference between the 2 ultrasound images taken before and during indentation during each condition. Crosssectional area measured in centimeter. 2 **P During abdominal brace contraction application, GS values increased, on average, 42.1% ( 52.3%) while MMS values increased 44.9% ( 41.6%). When both contractions were compared with each other, the abdominal brace contraction provided a significantly larger increase in PA spinal stiffness than the abdominal hollow contraction (Figures 6 and 7; P 0.02 and 0.01 for GS and MMS, respectively). No gender differences were found for either GS or MMS values (P 0.28, 0.78, respectively) for any of the 3 conditions. Further, there was no significant effect of age on GS (P 0.12) or MMS values (P 0.09). Discussion The results of the present study indicate that the abdominal brace and hollow contractions each increase immediate PA spinal stiffness when compared with resting PA stiffness values. When contraction types were compared with each other, the abdominal brace provided a greater immediate PA stiffening effect to the lumbar spine than the abdominal hollow. To our knowledge, this is the first study to directly quantify the immediate PA stiffening effects of these contractions in human subjects. Comparison to Previous Literature Our observation that the abdominal brace and hollow increased immediate PA spinal stiffness when compared with rest was consistent with findings from previous investigators who employed a range of different protocols including altered contraction intensities, 39,40 different testing locations, 7,39,41 alternate methods of stiffness assessment, 7,39 43 and animal models. 43 No effect of age or gender on PA spinal stiffness was noted in the present study although previous work has demonstrated gender differences, 42 which are likely explained by dissimilarity of testing protocols. Although it is apparent from previous studies that muscle contraction causes PA spinal stiffness to increase, these disparate protocols prevent comparison of the effect of different contraction strategies on PA spinal stiffness. Figure 5. EMG values for trunk muscles during rest, hollow, and brace conditions. For clarity, only significant differences between the hollow and brace condition are shown. No gender differences were found. **P 0.01.

6 Effect of Abdominal Stabilization Contractions on PA Spinal Stiffness Stanton and Kawchuk 699 Table 3. Expected and Observed Contraction of the Trunk Muscles for Each Condition: Rest, Hollow, and Brace Rest Hollow Brace Musculature TrA (CSA) Sup. Abs. ES TrA (CSA) Sup. Abs ES TrA (CSA) Sup. Abs ES Expected None None None 1 Min. Min Observed None None None 1 Min. None TrA indicates transversus abdominis; Sup. Abs, superficial abdominals consisting of rectus abdominis, external obliques, and internal obliques; ES, erector spinae musculature consisting of thoracic erector spinae and lumbar erector spinae; Min., minimum contraction. Table 4. Mean Stiffness Values Determined for All Individuals and Trials Contractions Mean Difference SE P GS 1 Rest Hollow Rest Brace Hollow Brace MMS 1 Rest Hollow Rest Brace Hollow Brace To rectify disparity between protocols, several previous studies have compared abdominal hollow and brace contractions directly. 7,19,20 Unfortunately, these studies do not apply directly to the in vivo human lumbar spine. Despite this limitation, a brief comparison of our results to these prior studies is warranted. Although limited to the SI joint, Richardson et al s observation that the abdominal hollow contraction increased joint stiffness more than the abdominal brace is directly opposite to our findings. The incongruity of these findings may be explained by several factors including anatomic differences in the TrA muscle between the lumbar and SI regions. 44,45 Although our findings are opposite to those of Richardson et al, they are in direct agreement with the findings of Grenier and McGill 19 and Vera-Garcia et al. 20 In each of these studies, the abdominal brace increased stability to a greater extent than the abdominal hollow. These results are explained not only by optimal computational conditions, but because the brace activates a greater number of muscles. Limitations and Assumptions Several cautions must be given when the results from this study are considered. PA stiffness is calculated from force and displacement data and is a measure used commonly by other investigators. 37,38,40,46 49 In our laboratory, this measure has been shown to have excellent validity 25,27 and reliability. 25a Other methods are also used to compute stiffness and/or stability and include vibration, 7 computational modeling 21,34,50,51 and in vitro approaches. 43 Given this range of measurement techniques, differences in variables such as loading rate and included tissues, caution is urged when comparing PA spinal stiffness values between studies. PA stiffness is a combined response of soft tissue deformation and rigid body displacement. 52 Prior work has demonstrated that a load of 100 N is able to cause vertebral displacement in animals with posterior tissue thicknesses much greater than those in humans. 52 Because these posterior tissues reduce much of the final load experienced directly by the vertebrae themselves, it can be assumed that vertebral deformation is not possible under these conditions. Figure 6. Mean ( SD) GS values for rest, hollow, and brace conditions. No gender differences were found. *P 0.05; **P 0.01.

7 700 Spine Volume 33 Number Figure 7. Mean ( SD) MMS values for rest, hollow, and brace conditions. No gender differences were found. *P 0.05; **P Although recent literature suggests a relationship between PA spinal stiffness and stability, 53,54 there is no single measure that objectifies spinal stability 55 as spinal stability is a multifactorial condition. Therefore, changes in the immediate spinal stiffness created by abdominal brace and hollow contractions cannot be considered to be indicative of a change in spinal stability. Finally, this work cannot be generalized to symptomatic subjects as it is unknown how the abdominal hollow and brace contractions may differ in these persons. Significance The present study contributes to our general knowledge about muscle activation in the torso in that we have shown that unique contraction patterns can be taught to an asymptomatic population and that these contraction patterns have different immediate effects on a specific measure of spinal stiffness. At this time, the clinical significance of the immediate effects of the abdominal hollow and brace are not known. Although it would be tempting to speculate that the brace contraction pattern may be more effective due to its ability to produce a greater stiffening effect, there is no current evidence that would help clinicians determine if the difference between these contraction strategies is clinically significant or if so, when a greater or lesser stiffening response is more desirable. Furthermore, this study, like others in this topic area, explored the immediate effect of muscular contraction on a measure of spinal stability. Future studies are required to understand the long-term effect of performing these contractions repeatedly. Key Points The abdominal hollow and the abdominal brace are 2 different combinations of trunk muscle contractions that are commonly prescribed to increase spinal stability. Unfortunately, the immediate effect of these different contractions on spinal stiffness (one indicator of spinal stability) has not yet been quantified directly. Both the abdominal hollow and abdominal brace contraction increased PA spinal stiffness significantly when compared with the rest condition. When the abdominal brace and hollow contractions were compared with each other, the abdominal brace contraction produced significantly greater PA spinal stiffness. Future work is required to assess the long-term effect of repeated abdominal brace and hollow contractions on PA spinal stiffness and low back pain. Acknowledgments The authors would like to thank Jessica Liddle, Teresa Waser, and Ian Matthew Jordan for their assistance. References 1. Luo X, Pietrobon R, Sun SX, et al. Estimates and patterns of direct health care expenditures among individuals with back pain in the united states. Spine 2004;29: CDC. MMWR. 2001;50: Bergquist-Ullman M, Larsson U. Acute low back pain in industry: a controlled prospective study with special reference to therapy and confounding factors. Acta Orthop Scand 1970;170: Troup JD, Martin JW, Lloyd DC. Back pain in industry: a prospective study. Spine 1981;6: Panjabi MM. The stabilizing system of the spine. part II. neutral zone and instability hypothesis. J Spinal Disord 1992;5: Richardson C, Jull G, Hodges P, et al. Therapeutic Exercise for Spinal Segmental Stabilization in Low Back Pain. 1st ed. London: Churchill Livingstone; Richardson CA, Snijders CJ, Hides JA, et al. The relation between the transversus abdominis muscles, sacroiliac joint mechanics, and low back pain. Spine 2002;27: Hodges PW, Cresswell AG, Daggfeldt K, et al. In vivo measurement of the effect of intra-abdominal pressure on the human spine. J Biomech 2001;34: Cresswell AG, Grundstrom H, Thorstensson A. Observations on intra-

8 Effect of Abdominal Stabilization Contractions on PA Spinal Stiffness Stanton and Kawchuk 701 abdominal pressure and patterns of abdominal intra muscular activity in man. Acta Physiologica Scandinavica 1992;144: Wilke HJ, Wolf S, Claes LE, et al. Stability increase of the lumbar spine with different muscle groups: a biomechanical in vitro study. Spine 1995;20: Hides JA, Jull GA, Richardson CA. Long-term effects of specific stabilizing exercises for first-episode low back pain. Spine 2001;26:E243 E O Sullivan PB, Twomey LT, Allison GT. Evaluation of specific stabilizing exercise in the treatment of chronic low back pain with radiologic diagnosis of spondylolysis or spondylolisthesis. Spine 1997;22: Hodges PW, Richardson CA. Inefficient muscular stabilization of the lumbar spine associated with low back pain. A motor control evaluation of transversus abdominis. Spine 1996;21: Hodges PW, Richardson CA. 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Mobilisation of the Spine: Notes on Examination, Assessment, and Clinical Method. 4th ed. Edinburgh; New York: Churchill Livingstone; Kawchuk GN, Fauvel OR. Sources of variation in spinal indentation testing: Indentation site relocation, intraabdominal pressure, subject movement, muscular response, and stiffness estimate. J Manipulative Physiol Ther 2001; 24: Teyhen DS, Miltenberger CE, Deiters HM, et al. The use of ultrasound imaging of the abdominal draw-in maneuver in subjects with low back pain. J Orthop Sports Phys Ther 2005;35: Abramoff MD, Magelhaes PJ, Ram SJ. Image processing with image J. Biophotonics Int 2004;11: McMeeken JM, Beith ID, Newham DJ, et al. The relationship between EMG and change in thickness of transversus abdominis. Clin Biomech 2004;19: Hides JA, Richardson CA, Jull GA. Magnetic resonance imaging and ultrasonography of the lumbar multifidus muscle: comparison of two different modalities. Spine 1995;20: Merletti R. Standards for reporting EMG data. J Electrophysiol Kinesiol Cholewicki J, McGill SM. Mechanical stability of the in vivo lumbar spine: implications for injury and chronic low back pain. Clin Biomech 1996;11: Kavcic N, Grenier S, McGill SM. Quantifying tissue loads and spine stability while performing commonly prescribed low back stabilization exercises. Spine 2004;29: Hodges P, Cresswell A, Thorstensson A. Preparatory trunk motion accompanies rapid upper limb movement. Exp Brain Res 1999;124: Brereton LC, McGill SM. Frequency response of spine extensors during rapid isometric contractions: effects of muscle length and tension. J Electromyogr Kinesiol 1998;8: Latimer J, Lee M, Goodsell M, et al. Instrumented measurement of spinal stiffness. Man Ther 1996b;1: Latimer J, Goodsell MM, Lee M, et al. Evaluation of a new device for measuring responses to posteroanterior forces in a patient population, part I: reliability testing. Phys Ther 1996c;76: Lee M, Esler MA, Mildren J, et al. Effect of extensor muscle activation on the response to lumbar posteroanterior forces. Clin Biomech 1993;8: Shirley D, Lee M, Ellis E. The relationship between submaximal activity of the lumbar extensor muscles and lumber posteroanterior stiffness. Phys Ther 1999;79: Colloca CJ, Keller TS. Active trunk extensor contributions to dynamic posteroanterior lumbar spinal stiffness. J Manipulative Physiol Ther 2004;27: Keller TS, Colloca CJ. In vivo transient vibration assessment of the normal human thoracolumbar spine. J Manipulative Physiol Ther 2000;23: Hodges P, Kaigle Holm A, Holm S, et al. Intervertebral stiffness of the spine is increased by evoked contraction of transversus abdominis and the diaphragm: in vivo porcine studies. Spine 2003;28: Urquhart DM, Barker PJ, Hodges PW, et al. Regional morphology of the transversus abdominis and obliquus internus and externus abdominis muscles. Clin Biomech 2005;20: Crisco JJ, Panjabi MM. The intersegmental and multisegmental muscles of the lumbar spine: a biomechanical model comparing lateral stabilizing potential. Spine 1991;16: Kawchuk GN, Fauvel OR, Dmowski J. Ultrasonic indentation: a procedure for the noninvasive quantification of force-displacement properties of the lumbar spine. J Manipulative Physiol Ther 2001;24: Edmondston SJ, Allison GT, Gregg CD, et al. Effect of position on the posteroanterior stiffness of the lumbar spine. Man Ther 1998;3: Lee M, Svensson NL. Measurement of stiffness during simulated spinal physiotherapy. Clinical Physics Physiological Measurement 1990;11: Lee R, Evans J. Load-displacement-time characteristics of the spine under posteroanterior mobilisation. Aust J Physiother 1992;38: Cholewicki J, Panjabi MM, Khachatryan A. Stabilizing function of trunk flexor-extensor muscles around a neutral spine posture. Spine 1997;22: Kavcic N, Grenier S, McGill SM. Determining the stabilizing role of individual torso muscles during rehabilitation exercises. Spine 2004;29: Kawchuk GN, Kaigle AM, Holm SH, et al. The diagnostic performance of vertebral displacement measurements derived from ultrasonic indentation in an in-vivo model of degenerative disc disease. Spine 2001;26: Childs JD, Fritz JM, Flynn TW, et al. A clinical prediction rule to identify patients with low back pain most likely to benefit from spinal manipulation: a validation study. Ann Intern Med 2004;141:920 8; W165 W Hicks GE, Fritz JM, Delitto A, et al. Preliminary development of a clinical prediction rule for determining which patients with low back pain will respond to a stabilization program. Arch Phys Med Rehabil 2005;86: Reeves NP, Narendra KS, Cholewicki J. Spine stability: the six blind men and the elephant. Clin Biomech 2007;22:

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