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    Ovid: Hodges: Spine, Volume 21(22).November 15, 1996.2640-2650

    Lippincott-Raven Publishers.

    Volume 21(22) 15 November 1996 pp 2640-2650

    Inefficient Muscular Stabilization of the Lumbar Spine Associated With Low Ba

    Pain: A Motor Control Evaluation of Transversus Abdominis[Article]

    Hodges, Paul W. BPhty(Hons); Richardson, Carolyn A. PhD

    From the Department of Physiotherapy, The University of Queensland, Australia.Supported by the Menzies Foundation, Physiotherapy Research Foundation, Dorothy Hopkins Award, all in

    Australia.Acknowledgment date: December 1, 1995.First revision date: May 10, 1996.Acceptance date: May 10, 1996.Device status category: 7.Address reprint requests to: Paul W. Hodges, BPhty(Hons);Department of Physiotherapy; The University oQueensland; Qld 4072; Australia

    Outline

    Abstract Motor Control of Lumbar Spine Stability Purpose of the Study

    [black small square] Methods [black small square] Results

    Non-LBP Subject Response

    LBP Subject Response Comparison of Groups

    [black small square] Discussion Normal Neuromotor Response of the Trunk Muscles Accompanying Limb Movement Dysfunction of Motor Control of the Trunk Muscles in Patients With Low Back Pain Potential Mechanisms for Temporal Delay in the Trunk Muscles Methodologic Considerations

    [black small square] Conclusion Acknowledgments

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    References

    Graphics

    Table 1 Figure 1 Table 2 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Table 3

    Abstract^

    Study Design: The contribution of transversus abdominis to spinal stabilization was evaluated indirectly inpeople with and without low back pain using an experimental model identifying the coordination of trunkmuscles in response to a disturbance to the spine produced by arm movement.

    Objectives: To evaluate the temporal sequence of trunk muscle activity associated with arm movement, and

    determine if dysfunction of this parameter was present in patients with low back pain.

    Summary of Background Data: Few studies have evaluated the motor control of trunk muscles or the potentor dysfunction of this system in patients with low back pain. Evaluation of the response of trunk muscles toimb movement provides a suitable model to evaluate this system. Recent evidence indicates that this

    evaluation should include transversus abdominis.

    Methods: While standing, 15 patients with low back pain and 15 matched control subjects performed rapidhoulder flexion, abduction, and extension in response to a visual stimulus. Electromyographic activity of th

    abdominal muscles, lumbar multifidus, and the contralateral deltoid was evaluated using fine-wire and surfa

    electrodes.

    Results: Movement in each direction resulted in contraction of trunk muscles before or shortly after the deltoin control subjects. The transversus abdominis was invariably the first muscle active and was not influenced

    by movement direction, supporting the hypothesized role of this muscle in spinal stiffness generation.Contraction of transversus abdominis was significantly delayed in patients with low back pain with allmovements. Isolated differences were noted in the other muscles.

    Conclusions: The delayed onset of contraction of transversus abdominis indicates a deficit of motor control

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    and is hypothesized to result in inefficient muscular stabilization of the spine.

    Dysfunction of the ventral and dorsal muscles of the trunk have been studied in relation to low backpain (LBP) for many years.6,23,40,41,57This has been based on the premise that insufficiency ofmuscle function leads to stress and undue load on the joints and ligaments of the spine.19,45,50

    However, despite considerable effort, few studies of muscular strength and endurance have identifia discernible and consistent abnormality of trunk muscle function in people with LBP.49Nevertheless, rehabilitation techniques advocating the training of muscular stabilization of the spineare purported to be effective,27,47,51indicating that additional components of the muscular system ohe lumbar spine require investigation. Although, many muscles of the trunk are capable of

    contributing to the stabilization and protection of the lumbar spine,3recent evidence has suggestedhat transversus abdominis (TrA) may be critically involved 11and has been the focus ofehabilitation.27,47Evaluation of the function of this muscle in people with LBP has not been

    addressed.

    The muscle fibers of TrA run horizontally around the abdomen, attaching via the thoracolumbarascia to the transverse processes of each of the lumbar vertebrae.60The increase in intra-abdomina

    pressure and tensioning of the thoracolumbar fascia resulting from contraction of this muscle initialwere thought to decrease spinal loading through the production of a trunk extensor moment.19,20Thheory has largely been refuted,36,38,56and consequently, it has been hypothesized that the

    contraction of TrA may enhance stabilization of the spine.10,39,56

    Farfan 15and McGill and Norman 39suggested that the contraction of the hoop-like TrA creates aigid cylinder, resulting in enhanced stiffness of the lumbar spine. Similarly, it may be expected thaateral tension through the transverse processes of the lumbar vertebrae would result in limitation ofranslational and rotational motion of the spine. Furthermore, the creation of a pressurized visceral

    cavity anterior to the spine results in the production of a force against the apex of the lumbar lordoswhich has been suggested to increase the stability of the structure of the spine for a variety of postuand movements.2The unexpected continuous activation of TrA throughout flexion and extension ohe trunk 10is consistent with this proposal. The consequence of dysfunction of TrA would beuboptimal control of the spine against forces acting to challenge the integrity of the spine.

    Motor Control of Lumbar Spine StabilityThe aspect of trunk muscle function that has received only limited attention in LBP research isevaluation of the motor control mechanisms.45A model for the evaluation of motor control strategior stabilization of the spine would necessarily involve identification of the coordination and timing

    of contraction of muscles contributing to spinal stiffness generation. On the basis of the previousarguement, TrA should be included.

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    Evaluation of the motor control of spinal stability is difficult because of the complex nature of theystem enabling it to deal with constantly changing demands as a function of continual variation innternal and external forces.45Evaluation of this system would be facilitated by identification of the

    muscular response to a controlled challenge to stability. Several studies have attempted to achievehis by investigation of the response of the spinal muscles to external loading of the trunk by havingubjects either catch a weight in their hands 28,31,37or by adding weight to a harness over theirhoulders,11indicating a rapid and often excessive response of the trunk muscles to control the

    disturbing force. In trials in which the loading was expected by the subject, the response preceded toading.11,31,32Using this model, Cresswell et al 11reported TrA to precede not only the acceptanc

    of the load but also the onset of the other trunk muscles, providing further support for the role of thimuscle in spinal stabilization.

    The muscular response to this type of external loading relies on the control of spinal stability againsorces in which the magnitude and direction are uncertain until the load is accepted, necessitating a

    gross general response of the trunk muscles and revealing little of the specificity expected of thepinal stabilizing system. Evaluation of the control strategy using a model in which the exact nature

    of the disturbance or perturbation can be anticipated by the central nervous system would facilitate more specific investigation of this complex system.

    Evaluation of the response of the body to movement of a limb provides such a model. In associationwith the change in the position of the center of mass produced by the limb displacement, dynamicorces are transmitted to the body by the inertial reactions between the segments.16Using this modehe influence of the reactive forces at the spine has been evaluated with unilateral and bilateral

    movement of the shoulder 61and elbow.16These studies either have calculated or recorded theproduction of a net flexion moment accompanying upper limb flexion and the converse withextension. Furthermore, unilateral limb movement also would be associated with a rotary moment.Accordingly, this disturbance to the stability of the spine and position of the center of mass of thebody is consistent and may be predicted by the central nervous system.7,16,25

    Many studies have used this model for evaluation of control of body equilibrium and have indicatedhat the body deals with these predictable disturbances by activation of lower limb muscles before tnitiation of the movement.5Contraction of muscles in this way has been termed anticipatory.1In th

    course of evaluating equilibrium control, several studies have identified contraction of rectus

    abdominis (RA) and erector spinae (ES) before the initiation of upper limb movement,1,16,61uggesting that spinal control may be dealt with in an anticipatory manner. It is important that thecontribution of muscles such as TrA be included in the evaluation of the muscular contribution tocontrol of the lumbar spine against self-generated perturbation and that the results compared withhose of a population with LBP.

    Purpose of the StudyThe objective of this research was to evaluate several hypotheses regarding the motor control of TrAand stabilization of the lumbar spine. Namely, it was hypothesized that contraction of TrA would

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    precede the initiation of limb movement and the other muscles of the trunk (consistent with the worof Cresswell et al).11Furthermore, considering the proposed mechanisms through which TrA maycontribute to stabilization of the spine, it was predicted that the response of this muscle would not bnfluenced by changes in the direction of the reactive forces. Finally, it was hypothesized that peopl

    with LBP would have disruption of this spinal stabilizing mechanism, which would fail to contractTrA before movement. Preliminary results have been published as an abstract,24and results of apreliminary study of a separate group of subjects without LBP is in preparation.

    [black small square] Methods^Subjects.Thirty subjects participated in the study including 15 patients (eight male, seven female)with a history of lumbar spine pain and 15 age- and sex-matched control subjects. All patients withLBP were medically screened to rule out back pain of nonmusculoskeletal etiology. Recruitment ofhe subjects with LBP was based on strict clinical criteria of chronicity and severity. This basis forubject selection was necessary because of the difficulty in obtaining a homogenous subject group ohe basis of current investigative techniques, which are unable to identify a definitive cause for the

    pain in the majority of patients.42For inclusion in the pain group, the subjects were required to havLBP of insidious onset of at least 18 months duration for which they had sought medical or alliedhealth treatment. The pain was to be of sufficient intensity to cause them to restrict their activity,nvolving a minimum of 3 days absent from work and be episodic with at least one painful episode

    per year or of a semicontinuous nature with periods of greater and minimal pain. The subjects werehave minimal or no pain at the time of testing. The mean duration of symptoms was 8.6 years (rang2-30 years), and time off work was 9 days (range, 3-40 days). Subjects were excluded if they hadneurologic symptoms, observable spinal deformity (e.g., scoliosis), previous lumbar surgery,neuromuscular or joint disease, or if they had undertaken abdominal or back muscle training in the

    months before testing. Habitual physical activity was measured using a questionnaire developed anvalidated by Baecke et al.4The demographic data and habitual activity data for both subject groupsare presented in Table 1. The study was approved by the Medical Research Ethics Committee of TheUniversity of Queensland.

    Table 1. Demographic Data for the Control and LBP Groups (Mean SD)

    Experimental Design.The design of this research aimed to provide a model for the evaluation of thcontrol of stability of the spine in response to a self-generated perturbation to the spine in controlubjects and those with LBP. The model, modified from a paradigm commonly used to identify

    central nervous system control of body equilibrium,5,7involved the identification of the timing ofonset of electromyographic (EMG) activity of the abdominal and the lumbar multifidus muscles inassociation with rapid movement of an upper limb in response to a visual stimulus (Figure 1). Theelationship between the action of the muscles and the direction of the reactive forces was evaluated

    by performance of limb movement in each of three directions. Two parameters associated withpecific LBP populations, namely reduced limb movement velocity 59and certain postural

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    deviations,29,54are known to influence anticipatory postural reactions.25,33,34Measurement of bothhese factors was performed in a separate session to identify if variation existed between groups tha

    could explain the hypothesized changes in the anticipatory trunk muscle response with LBP.

    Figure 1. Experimental model for the evaluation of the trunk muscle response to rapid movement o

    he upper limb.

    Electromyographic Recordings. A combination of fine-wire and surface EMG electrodes were usedBipolar fine-wire electrodes were fabricated from Teflon-coated stainless steel wire (75 m, 1 mmnsulation removed; A-M System Inc., Everett, WA) inserted into a bevelled-edged hypodermic

    needle (0.70 32mm) and bent back sharply against the needle, leaving the receptive ends staggereat 1.5 and 3 mm. All fine-wire electrodes were inserted under the guidance of real-time ultrasoundmaging (Advanced Technology Laboratory, Bothel, WA) using a 5-MHz curved array sound head

    This technique has been described in detail elsewhere.10Electrode insertion was preceded by the

    application of anesthetic EMLA cream (Astra Pharmaceuticals, North Ryde, NSW, Australia). Ag/AgCl bipolar surface electrodes were used with an interelectrode distance of 12 mm. EMG data weampled at a rate of 2000 Hz with 12-bit analog to digital conversion and bandpass filtered at 20-10

    Hz. All data were stored on computer for later analysis.

    The fine-wire electrodes were inserted into the left TrA, obliquus abdominis internus (IO), andobliquus abdominis externus (EO) at standard sites: TrA 2 cm anterior to the proximal end of a linedrawn vertically from the anterior superior iliac spine (ASIS) to the rib cage; IO 2 cm medical anduperior to the ASIS; and EO midway between the iliac crest and rib cage in the mid-axillary line.

    Confirmation of placement was achieved by gentle traction of the wire and visualization of movemusing the ultrasound. Surface electrodes were positioned: centrally over the muscle bellies of theanterior, middle, and posterior portions of the right deltoid muscle parallel with the muscle fibers; Reither side of a line joining the right and left ASIS 2 cm lateral to the midline; left lumbar multifiduMF) at the L4-L5 interspace 2 cm lateral to the spinous process. The ground electrode was placed

    over the right ASIS. Before attachment, the skin was prepared in a standard manner to reduce the skmpedance below 5 k[OMEGA].

    Procedure. The experimental procedure was identical for the LBP and control groups. To standardi

    he test position, the subject stood on a Balance Performance Monitor (SMS Healthcare, UK) (Figurehat provided auditory feedback of right-left weight inequality. Furthermore, the EMG activity of thmuscles evaluated was monitored throughout the procedure, and the subjects were encouraged toelax consciously if the degree of muscle activity increased above a resting level. Both subject grou

    were able to achieve this criteria.

    Ten repetitions each of shoulder flexion and abduction to approximately 60 and extension toapproximately 40 were performed as fast as possible in response to the visual command. Theemphasis was on speed of limb movement rather than accuracy. The visual command to move was

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    provided by a series of light-emitting diodes situated 1.5 m in front of the subject at eye level. Awarning stimulus was illuminated before the stimulus moved to focus the attention of the subject. Tperiod between the two lights was varied randomly between 0.5-4 msec to eliminate the possibilityhat the subject could anticipate the timing of the second stimulus.46The order of movement

    directions was randomized, and the subject adopted a seated position for 5 minutes between eachdirection of movement. No pain was experienced by any of the subjects with LBP during testing.

    Limb Movement Velocity Study. Five subjects were selected randomly from each group for the limbmovement velocity evaluation. The velocity measurements were made using a Position VelocityTransducer (UniMeasure, Corvallis, Oregon), which records the linear velocity of distraction of acable from the transducer. Using trigonometric calculations, it was possible to convert the linearvelocity to an angular velocity around the shoulder joint. It was necessary to exclude measurement imb movement speed from the EMG trials because the slight resistance provided by the cable at thnitiation of movement may influence the postural muscle response.16A strap was placed around thorearm 0.5 m from the tip of the acromion for attachment of the cable, and the device was position

    behind the subject with the distance from the acromion to the device measured for the calculation.

    Ten repetitions of shoulder flexion only were recorded using identical instructions to those used forhe EMG session. Data were sampled at 100 Hz, and the mean and peak velocity averaged over 10epetitions were used for the analysis.

    Postural Evaluation. The evaluation of lumbar lordosis and pelvic tilt was undertaken in the standinposition in a separate session several days after the EMG trial.

    Lumbar lordosis was measured using two pleurimeter gravity-dependent goniometers (Dr. RippsteiPleurimeter-Goniosystem, La Conversion, Switzerland) mounted on base plates and placed over the

    T11-T12 and L5-S1 interspace. The angle of curvature was calculated using a method described byToppenberg,58involving simple geometry to derive the angle of curvature of the spine.

    Pelvic tilt was evaluated as the angle of inclination measured between the right anterior and posteriliac spines using a plurimeter placed on a caliper with the tips of the arms of the device placed ovehe superior iliac spines.

    Data Analysis.The evaluation of timing of onset of EMG activity was conducted by computer, usian algorithm modified from that used by Di Fabio.13The EMG data were full-wave rectified, filterewith a 50-Hz sixth order elliptical low-pass filter, and then analyzed using MATLAB (The Math-Works, Natick, MA) software to identify the point where the mean amplitude of 50 consecutiveamples (25 msec) exceeded the mean baseline activity by two standard deviations. The mean of th

    baseline was calculated from the 50 msec before the warning stimulus. Each onset time was checkevisually to identify trials in which the onset was disrupted by a heart beat or movement artifact. Theime between the onset of contraction of each of the trunk muscles and the prime mover of the limb

    e., the difference time, formed the basis of the analysis. Consistent with previous studies, the onset runk muscle activity up to 50 msec after the onset of activity of the prime mover of the limb was

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    egarded as anticipatory.1These criteria are based on the finding that the initiation of limb movemenever occurs before 30 msec after the onset of activity of the prime mover of the limb because ofelectromechanical delay,43and therefore, any activity occurring before or shortly after this pointcannot be reflexly mediated.

    Comparison between individual trunk muscles, between movement directions, and between subjectgroups involved analysis of variance (ANOVA) statistics and Duncan's multiple range test.

    [black small square] Results^Non-LBP Subject ResponseWhen subjects without LBP flexed their shoulder, TrA was invariably the first muscle active,preceding the contraction of the anterior portion of the deltoid muscle (Figure 2 and Table 2). The reactiime for anterior deltoid with shoulder flexion was 188 32 msec. Each of the trunk muscles

    evaluated, other than TrA, followed the onset of anterior deltoid by 9-84 msec and was significantlydifferent to TrA. No significant difference was noted between MF and IO, IO and EO, or EO and R

    The onset of EO and RA occurred more than the 50 msec after the onset of the prime mover, makint impossible to rule out the possibility that the contraction of these muscles was reflexly mediated.

    Table 2. Time Between Onset of EMG Activity of the Trunk Muscles and the Prime Mover of

    he Limb (Mean SD) for the LBP and Control Subjects*

    Figure 2. Electromyographic (EMG) data of a representative control subject for all muscles averageover 10 repetitions for shoulder movement in different directions. The time of alignment of the tracat the onset of EMG activity of the prime mover is noted by the heavy dashed line at zero. The onseof TrA is noted by the fine dashed line. Note the onset of contraction of TrA before the other trunkmuscles, and the change in sequence of RA, EO, IO, and MF as a function of limb movementdirection. EMG is in arbitrary units. AD = anterior deltoid; MD = middle deltoid; PD = posteriordeltoid.

    Abduction of the shoulder similarly resulted in contraction of TrA before the prime mover of the limmiddle deltoid; Figure 2 and Table 2). The middle deltoid was active 171 54 msec after the movementimulus. In contrast to shoulder flexion, the onset of IO also occurred before the prime mover and

    was not significantly different from TrA. The contraction of EO shortly after the prime mover wasnot significantly different from either of these muscles. Contraction of RA and MF followed theprime mover and were not significantly different from each other. The onset of MF occurred morehan 50 msec after the prime mover and did not fulfill the anticipatory criteria.

    Shoulder extension was associated with contraction of TrA and RA before the posterior portion of t

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    deltoid (Figure 2 and Table 2). The latency between these muscles and the prime mover were not differeo each other nor were they significantly different to the difference time of IO, which became activehortly after the prime mover. EO and MF followed the onset of activity of the prime mover and we

    not significantly different from each other. The reaction time of posterior deltoid was 171 34 msewith shoulder extension. The onset of MF occurred outside the 50 msec anticipatory criteria.

    When the each of the different movement directions was compared, no significant difference was

    noted between the reaction time of the muscle responsible for movement of the limb (F14.2 = 1.27;= 0.29). However, because the sequence of activation of the trunk muscles varied between movemedirections, the latency between the prime mover and each of the muscles was not consistent betweedirections for the majority of muscles for the control subjects (Figure 3). The difference time for IOF14.2 = 4.62; P= 0.05), EO (F14.2 = 3.53, P< 0.05), RA (F14.2 = 16.17; P< 0.01), and MF (F14

    = 17.25, P< 0.01) varied between directions. IO and EO were active later relative to the prime movwith shoulder flexion compared with the other movement directions; the onset of RA wasignificantly different between all movement directions being active earliest in shoulder extension

    and latest in shoulder flexion; and MF was active significantly earlier in shoulder flexion than the

    other two directions of movement. In contrast, no significant difference was recorded for TrA (F14= 1.84; P= 0.18) across movement directions, indicating that the contraction of TrA was notnfluenced by the direction of the reactive forces.

    Figure 3. Control group mean (filled boxes) and individual subject (joined dots) times of onset ofelectromyographic (EMG) activity of each of the trunk muscles relative to the onset of the primemover of the limb with movement in different directions. Time of alignment is the onset of the prim

    mover at zero, denoted with the dashed line. The individual muscle is shown in the upper right cornNote the consistent time of onset of EMG activity of TrA across movement directions and theignificant differences in the other trunk muscles. F = flexion; A = abduction; E = extension). *P