Journal of Electromyography and Kinesiology xxx (2015) xxx–xxx

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Journal of Electromyography and Kinesiology

journal homepage: www.elsevier .com/locate / je lek in

Does insertion of intramuscular electromyographic electrodes altermotor behavior during locomotion?

http://dx.doi.org/10.1016/j.jelekin.2015.01.0031050-6411/� 2015 Elsevier Ltd. All rights reserved.

⇑ Corresponding author.

Please cite this article in press as: Armour Smith J, Kulig K. Does insertion of intramuscular electromyographic electrodes alter motor behavior durinmotion?. J Electromyogr Kinesiol (2015), http://dx.doi.org/10.1016/j.jelekin.2015.01.003

Jo Armour Smith ⇑, Kornelia KuligDivision of Biokinesiology and Physical Therapy, University of Southern California, 1540 East Alcazar Street, CHP-155, Los Angeles, CA 90089, United States

a r t i c l e i n f o a b s t r a c t

Article history:Received 13 September 2014Received in revised form 1 December 2014Accepted 6 January 2015Available online xxxx

Keywords:Intramuscular electromyographyLow back painLocomotionEquivalence testingFear avoidance

Intramuscular electromyography (EMG) is commonly used to quantify activity in the trunk musculature.However, it is unclear if the discomfort or fear of pain associated with insertion of intramuscular EMGelectrodes results in altered motor behavior. This study examined whether intramuscular EMG affectslocomotor speed and trunk motion, and examined the anticipated and actual pain associated withelectrode insertion in healthy individuals and individuals with a history of low back pain (LBP). Beforeand after insertion of intramuscular electrodes into the lumbar and thoracic paraspinals, participants per-formed multiple repetitions of a walking turn at self-selected and controlled average speed. Low levels ofanticipated and actual pain were reported in both groups. Self-selected locomotor speed was significantlyincreased following insertion of the electrodes. At the controlled speed, the amplitude of sagittal planelumbo-pelvic motion decreased significantly post-insertion, but the extent of this change was the samein both groups. Lumbo-pelvic motion in the frontal and axial planes and thoraco-lumbar motion in allplanes were not affected by the insertions. This study demonstrates that intramuscular EMG is an appro-priate methodology to selectively quantify the activation patterns of the individual muscles in theparaspinal group, both in healthy individuals and individuals with a history of LBP.

� 2015 Elsevier Ltd. All rights reserved.

1. Introduction

Intramuscular or fine-wire electromyography (EMG) iscommonly used to quantify the activity of the trunk musculatureduring static or dynamic motor tasks. In particular, intramuscularEMG methodology is often employed in research investigatingalterations in postural control of the trunk in individuals withlow back pain (LBP) (MacDonald et al., 2009; Tsao et al., 2011;Hall et al., 2009). Intramuscular EMG electrodes enable the mea-surement of activity in the deep muscles of the trunk that arenot accessible to surface EMG electrodes. These include the inter-nal oblique, transversus abdominis and the deep fibers of thelumbar multifidus (Beneck et al., 2013; MacDonald et al., 2009).In the paraspinal muscle group, the use of intramuscular EMG alsominimizes potentially confounding cross-talk from adjacent mus-culature that may have a different functional role (Lee et al., 2009).

However, a potential disadvantage of intramuscular EMG is thatthe pain associated with the insertion of the electrodes may altermotor behavior (MacDonald et al., 2009). For example, Younget al., (Young et al., 2004) demonstrated that in children with cere-bral palsy, self-selected locomotor speed, cadence, and step length

significantly decreased following insertion of intramuscular elec-trodes into the lower extremities. Similarly, Jacobson et al.,(Jacobson and Gabel, 1995) reported that after intramuscular elec-trode insertions into the vastus medialis and biceps femoris, two oftheir healthy adult subjects had an antalgic gait pattern duringwalking and running and two others required a break in testingdue to anxiety. Despite the large number of studies utilizing thismethodology, to date it has not been established whether insertingintramuscular EMG electrodes into the paraspinal muscles alterstrunk control or locomotor kinematics.

It is clear however that in healthy individuals, experimentallyinduced pain in the paraspinals alters postural control of the trunkduring standing and walking (Moseley et al., 2004; Lamoth et al.,2004; Arendt-Nielsen et al., 1995; Moe-Nilssen et al., 1999). Thesechanges in postural control during experimental pain are on thewhole suggestive of a ‘‘guarding’ or splinting strategy to reducemotion in the painful area (Moe-Nilssen et al., 1999; Lamothet al., 2004). Trunk control is also affected by the anticipation ofpain in the low back, even in the absence of actual pain itself(Moseley et al., 2004). However, as studies that utilize intramuscu-lar EMG in the trunk do not routinely quantify the level of painassociated with this methodology, it is unclear whether discomfortfollowing insertion is of sufficient intensity or duration to elicit

g loco-

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changes in motion in the trunk during motor activities after theelectrode insertions. Individuals with a history of LBP may have amore pronounced response to the insertion of intramuscular elec-trodes than healthy individuals due to elevated fear avoidancebehaviors or lowered pain thresholds (Imamura et al., 2013;Wand et al., 2011). Therefore, it is also important to determine ifthe magnitude of any change in motion in response to electrodeinsertion is the same in healthy individuals and individuals witha history of LBP.

Turning during walking is a common locomotor perturbation.Walking turns can be performed in the direction either ipsilateralto or contralateral to the stance limb. In comparison with steady-state locomotion, ipsilateral walking turns are associated withgreater postural demand (Taylor et al., 2005) and increased parasp-inal muscle activation (Armour Smith & Kulig, unpublished data).As a result, analysis of walking turns may provide greater insightinto changes in locomotor kinematics in response to intramuscularEMG insertion than steady-state locomotion. Therefore, theprimary purpose of this study was to investigate if insertion ofintramuscular EMG electrodes into the paraspinal musculature inhealthy individuals and individuals with a history of recurrentlow back pain resulted in reduced locomotor speed and reducedamplitude of trunk motion during ipsilateral walking turns. Wehypothesized that there would be no difference in locomotor kine-matics following electrode insertion. The secondary purpose of thisstudy was to quantify the anticipated and actual amount of painassociated with insertion of intramuscular electrodes into theparaspinal muscles.

2. Methods

2.1. Participants

Twenty-nine young adults between the ages of 22 and 31 yearsparticipated in the study (17 women, 12 men). Participants wererecruited via word of mouth and study flyers. Control participants(CTRL) were individually matched to participants with recurrentLBP (RLBP) by age (±five years), height in m (±10%) weight in kg(±10%) and activity level in metabolic equivalents (METS, ±15%;Table 1). Physical activity level was quantified using the PhysicalActivity Scale (Aadahl and Jorgensen, 2003). One participant witha history of recurrent LBP did not complete the data collectiondue to a transient episode of vasovagal syncope in response tothe intramuscular EMG insertion. Therefore only the remainingfourteen participants with a history of recurrent LBP were matchedto control participants. The Institutional Review Board of the Uni-versity of Southern California approved the procedures in thestudy. Participants gave written informed consent after a fullexplanation of the study procedures and the potential benefitsand risks of participating.

Participants were included in the RLBP group if they werebetween 18 and 40 years of age, had a history of more than oneyear of recurrent episodes of primarily unilateral LBP, reported atleast two functionally limiting pain episodes of at least 24 hours’

Table 1Participant demographics (median ± inter-quartile range).

CTRLa RLBPa p

Age (years) 24.5 ± 1.75 26.5 ± 4.75 .068Height (m) 1.73 ± 0.05 1.73 ± 0.09 .664Mass (kg) 66.68 ± 14.97 67.70 ± 23.42 .152PAS score (MET-time) 47.60 ± 5.00 48.20 ± 7.55 .470

a n = 14.

Please cite this article in press as: Armour Smith J, Kulig K. Does insertion of intrmotion?. J Electromyogr Kinesiol (2015), http://dx.doi.org/10.1016/j.jelekin.20

duration in the preceding year (Stanton et al., 2009), and were insymptom remission at the time of the data collection (defined asa score of less than 0.5/10 cm on a visual analogue scale (VAS)for current pain at the start of the data collection). Participantswere eligible for inclusion in the control group if they could beindividually matched to a participant in the RLBP group as previ-ously described and did not have any history of LBP requiring mod-ification of activity or medical care. Participants in both groupswere excluded if they had a history of diabetes mellitus, rheumaticjoint disease, any blood-clotting disorder or current anti-coagulanttherapy, polyneuropathy, history of low back surgery, history ofbilateral leg pain, spinal stenosis or scoliosis, spinal malignancyor infection, lumbar radiculopathy, current or previous musculo-skeletal injury or surgery affecting locomotion, or were currentlypregnant.

2.2. Assessment of symptoms

In the RLBP group, fear avoidance beliefs were quantified usingthe physical activity sub-scale of the Fear Avoidance Beliefs Ques-tionnaire (FABQ) (George et al., 2010). All participants completed abaseline VAS for current pain, anchored at 0 with ‘‘no pain’’ and at10 with ‘‘worst possible pain’’ (Carlsson, 1983). At baseline, partic-ipants also completed a VAS for the amount of pain they antici-pated feeling during the electrode insertions and the amount ofpain that they anticipated feeling during the locomotor trials fol-lowing the insertions (Al-Obaidi et al., 2003). Immediately afterthe electrode insertions they completed a further VAS for theactual amount of pain they felt during the insertions, and at theend of the data collection they completed a VAS for the actualamount of pain they felt during the locomotor trials that followedthe insertions.

2.3. Experimental task

Each locomotor trial consisted of three laps of a walking circuit.The circuit required both straight locomotion and a series of walk-ing turns (Fig. 1). Participants performed the circuit both at arelaxed, self-selected speed (SELF) and at a controlled averagespeed of 1.5 m/s ± 5% (FAST). Average speed was measured fromthe time taken to complete the standardized length of the circuitand was measured using photo-electric triggers. Participants exe-cuted an ipsilateral pivot turn in the same location in each repeti-tion of the circuit. They stepped into an outlined 70 cm by 70 cmarea with the foot ipsilateral to the turn direction and turnedbriskly 90� to the ipsilateral side (Fig. 1a). The strategy used to per-form the other walking turns in the circuit was not specified. Eachparticipant practiced the circuit until they were consistently ableto achieve the correct foot placement for the turn without lookingdown or breaking stride. At least seven successful trials of the cir-cuit at each speed were collected for each participant, resulting in atotal of at least 21 ipsilateral pivot turns in the defined turning areafor analysis for each condition (Fig. 1b). All participants walked thecircuit in the direction contralateral to the side of their EMGinstrumentation.

2.4. Instrumentation

Participants were first instrumented with motion-capturemarkers. Retro-reflective markers were attached to anatomicallandmarks to define body segments and joint axes. Rigid kinematicmodels of the pelvis and the lumbar and thoracic regions of thespine were defined using individual markers bilaterally on theanterior superior iliac spines, iliac crests, greater trochanters andon the L5/S1 disc space (pelvis), a rigid triad of markers affixed overthe spinous process of L1 (lumbar spine) and a rigid triad of

amuscular electromyographic electrodes alter motor behavior during loco-15.01.003

Fig. 1. (a) Schematic of the walking circuit, with the turning area for the ipsilateralpivot turn indicated. Circuit set up for participant instrumented on the left side andtherefore turning toward the right. (b) Stride cycle of an ipsilateral pivot turn to theright.

J. Armour Smith, K. Kulig / Journal of Electromyography and Kinesiology xxx (2015) xxx–xxx 3

markers over the spinous process of T3 (thoracic spine) (Popovichand Kulig, 2012). Wireless force-sensitive resistor foot switcheswere also attached bilaterally to the sole of participants’ shoesunder the lateral heel and the first metatarsophalangeal joint(TeleMyo DTS Telemetry, Noraxon USA Inc., Scottsdale, USA).

SP

H

Fig. 2. Axial ultrasound image (left) and schematic (right) demonstrating insertion of i(SP = spinous process, H = hypodermic needle).

Please cite this article in press as: Armour Smith J, Kulig K. Does insertion of intrmotion?. J Electromyogr Kinesiol (2015), http://dx.doi.org/10.1016/j.jelekin.20

Kinematic data were collected using an 11-camera digital motioncapture system sampling at a frequency of 200 Hz (Qualisys AB,Gothenburg, Sweden). After instrumentation with the motion cap-ture markers and footswitches, participants performed the first setof walking trials at both self-selected (pre-insertion SELF) and con-trolled speed (pre-insertion FAST).

We then performed the fine-wire EMG insertions, leaving themotion capture markers in situ. Fine-wire intramuscular electrodeswere inserted into the deep fibers of the lumbar multifidus at thelevel of L4, the longissimus thoracis pars lumborum at the levelof L4, and the longissimus thoracis pars thoracis at the level ofT10 using a previously described protocol with real-time ultra-sound imaging guidance (Beneck et al., 2013) (see Fig. 2 8 MHz lin-ear transducer, SONOLINE Antares™, Siemens Medical SolutionsInc., USA; nickel chromium alloy wires, 50 lm gauge, polyure-thane/nylon coating, tips bent back 5 and 3 mm with 2 mm wireexposed, 25 gauge hypodermic needles). Electrodes were insertedinto the predominant side of pain reported by participants with ahistory of RLBP and the same side for their matched control. Theneedle was immediately removed following the electrode inser-tion. Correct electrode placement was confirmed observing thecontraction induced by light electrical stimulation using ultra-sound imaging.

The electrodes were connected to wireless differential pream-plifiers (TeleMyo DTS Telemetry, Noraxon USA Inc., Scottsdale,USA: baseline noise <1 lV RMS, Input impedance > 100 Mohm,CMR > 100 dB, Input range ± 3.5 mV, Base gain 400). The EMGand foot switch data were transmitted via a wireless receiver (Tele-Myo DTS Telemetry, Noraxon USA Inc., Scottsdale, USA), digitallysampled at 3000 Hz at 16 bit resolution and synchronized withthe kinematic data using photoelectric triggers (Qualisys TrackManager v2.6, Qualisys AB, Gothenburg, Sweden). Immediatelyafter the fine-wire EMG insertions, participants walked freelyaround the laboratory to allow any residual soreness or anxietyto dissipate. They then performed a second set of walking circuittrials at both self-selected and controlled speed (post-insertionSELF and FAST respectively).

2.5. Data processing

Between 15 and 21 turning trials were analyzed for each partic-ipant for each condition. Kinematic data were first processed usingVisual3D™ software (C-Motion Inc., MD, USA) before beingexported to MATLAB

�(MathWorks, MA, USA) for further analysis.

Marker trajectories were low-pass filtered with a 10 Hz recursivefourth order Butterworth filter (Angeloni et al., 1994). The stride

Spinousprocess

ntramuscular EMG electrode into the deep fibers of the lumbar multifidus muscle

amuscular electromyographic electrodes alter motor behavior during loco-15.01.003

Table 2Visual analogue scores for anticipated and actual pain associated with intramuscularEMG electrode insertion (Median ± inter-quartile range, n = 28).

CTRL RLBP p

Anticipated painduring insertionsa 1.35 ± 2.43 1.90 ± 1.63 .730during locomotor trialsa 0.60 ± 0.78 0.50 ± 0.35 .937

Actual painduring insertionsa 2.45 ± 2.65 1.90 ± 2.38 .753during locomotor trialsa 0.45 ± 0.70 0.50 ± 0.70 .779

a VAS scale scores in cm.

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cycle of each ipsilateral pivot turn (Fig. 1b) was determined usingthe voltage signals of the foot switches and confirmed with a visualcheck of the horizontal velocity of a motion capture marker posi-tioned on the posterior heel. Local coordinate systems for each seg-ment, relative to the global laboratory coordinate system, weredetermined from a standing calibration trial. Segment and jointkinematics were then calculated across the turn stride cycle usingCardan angles and a rotation order of XYZ (flexion/extension;abduction/adduction; axial rotation; Schache et al., 2002). Thealignment of the lumbar and thoracic segments was normalizedto the static standing trial to account for individual postural align-ment (Popovich and Kulig, 2012). Average peak-to-peak amplitudeof angular lumbo-pelvic and thoraco-lumbar motion in all planesduring the walking turns at the controlled speed (FAST) was calcu-lated for each participant. Average self-selected walking speed dur-ing the walking circuit pre- and post-insertion was calculated foreach participant from the time taken to complete each locomotortrial. Average duration of the turn stride cycle at the controlledspeed was also determined in order to compare the speed thatthe turn was executed pre- and post-insertion. The ensemble aver-age for the RLBP and CTRL groups for all variables was thencalculated.

2.6. Statistical analysis

The dependent variables that were compared pre and post-intramuscular EMG electrode insertion were (i) average self-selected walking speed (pre-and post-insertion SELF); (ii) durationof the turn stride cycle at the controlled speed (pre- and post-insertion FAST); (iii) amplitude of peak-to-peak lumbo-pelvic andthoraco-lumbar motion in all planes at controlled walking speed(pre- and post-insertion FAST). The extent of change in each vari-able from pre- to post-insertion was compared between the RLBPand CTRL groups using paired t-tests (parametric data) and Wilco-xon signed ranks tests (non-parametric data). To correct for multi-ple comparisons a Bonferroni correction was used resulting in alevel of significance set at a = 0.0063. Additionally, anticipatedand actual pain during the insertions and during the post-insertionwalking trials was compared using Wilcoxon signed rank tests.

Inferential confidence intervals were used to determinewhether the variables were equivalent in the pre- and post-inser-tion conditions, or if there was a significant change in the variablesfrom the pre- to post-insertion (Tryon, 2001; Stegner et al., 1996).This approach was used because equivalence between two condi-tions is not proven simply by a failure to reject the null hypothesisusing a standard hypothesis-testing approach. Testing equivalenceusing an inferential confidence interval approach avoids the prob-lem of the likelihood of being able to demonstrate equivalenceactually becoming smaller as the study variance decreases(Stegner et al., 1996), and also defines a priori an amount of changein the variable that is considered to be meaningful (Tryon, 2001). Ifthe difference between the lower limit of the 95% confidence inter-val for the smaller of the pre- and post-insertion means and theupper limit of the 95% confidence interval for the larger of thetwo means falls within the pre-defined range of equivalence forthat variable, no statistically significant or meaningful change inthe variable has occurred (Tryon, 2001). Conversely, if there is nooverlap between the inferential 95% confidence intervals for thetwo means, there is a statistically significant difference in the var-iable from pre- to post-insertion at the p = 0.05 level. For this study,the range of equivalence was defined as ±the minimal detectablechange (MDC) for each of the variables. MDC for self-selected walk-ing speed was determined by having five healthy individualsperform two blocks of trials of the locomotor circuit at a self-selected speed, separated by a period of relaxation of approxi-mately 15 min. MDC for the kinematic variables was determined

Please cite this article in press as: Armour Smith J, Kulig K. Does insertion of intrmotion?. J Electromyogr Kinesiol (2015), http://dx.doi.org/10.1016/j.jelekin.20

by having four healthy individuals perform two blocks of trials ofthe locomotor circuit at the controlled speed. The two blocks of tri-als were separated by a period of approximately 15 min duringwhich they performed a different sub-maximal motor task(straight walking). Intra-class correlation coefficients (ICC3,1) andthe standard error of the measure (SEM) were calculated for eachvariable. MDC was then determined using the equationMDC = 1:96�p2� SEM (King, 2011). All statistical analyses wereperformed using PASW Statistics (Version 18, IBM Corp., Armonk,NY).

3. Results

Average duration of symptoms in the RLBP group was5.8 ± 4.2 years. At baseline, average current pain was0.12 ± 0.24 cm in the participants with a history of RLBP and0.0 cm in the healthy controls. Median ± inter-quartile range FABQphysical activity score in the RLBP group was 12.50 ± 6.7.

3.1. Anticipated and actual pain associated with EMG electrodeinsertion

The anticipated and actual pain VAS scores for EMG insertionand locomotor trials are shown in Table 2. There was no significantdifference between groups for any of the VAS scores (Table 2).

3.2. Effects of intramuscular EMG electrode insertion

Due to problems with marker occlusion during the pre-inser-tion trials for one participant in the RLBP group, the data from thisparticipant and the matched control participant were not includedin data analysis, leaving a sample size of 26. There were no signif-icant differences between the RLBP and CTRL groups in the extentof change in any of the variables in response to electrode insertion(SELF walking speed group comparison p = .369; FAST stride dura-tion p = .260; FAST lumbo-pelvic motion sagittal plane p = .643,frontal plane p = .854, axial plane p = .276; FAST thoraco-lumbarmotion sagittal plane p = .807, frontal plane p = .279, axial planep = .237). Therefore the inferential confidence intervals were calcu-lated using the pooled data from both groups.

The controlled speed was faster than the self-selected speed inall individuals except one CTRL participant. Self-selected walkingspeed significantly increased after the insertion of intramuscularEMG electrodes (mean ± standard deviation, pre-insertion SELF1.l5 ± 0.14 m/s, post-insertion SELF 1.22 ± 0.12 m/s, Fig. 3a). Atthe controlled speed, there was no difference in the duration ofthe stride cycle between pre- and post-insertion (pre-insertionFAST 1.03 ± 0.05 s, post-insertion FAST 1.02 ± 0.06 s, Fig. 3b).

In the sagittal plane, the peak-to-peak amplitude of lumbo-pel-vic motion across the turn stride cycle decreased significantly frompre- to post-insertion (pre-insertion FAST 9.56 ± 2.30�, post-inser-tion FAST 8.45 ± 2.19�, Fig. 4a). This decrease in the amplitude ofsagittal lumbo-pelvic motion occurred in the majority of partici-pants in both groups (CTRL n = 10, RLBP n = 10) and was due to

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reduced peak flexion in 7 participants, reduced peak extension in 7participants, and a reduction in both peak flexion and extension in6 participants. There was no change in lumbo-pelvic frontal motion(pre-insertion FAST 5.77 ± 1.58�, post-insertion FAST 5.37 ± 1.32�)or lumbo-pelvic axial motion (pre-insertion FAST 8.24 ± 1.75�,post-insertion FAST 8.85 ± 1.90�, Fig. 4a). Thoraco-lumbar motionin all planes was equivalent pre and post-insertion (sagittal planepre-insertion FAST 5.36 ± 1.04�, post-insertion FAST 4.86 ± 1.26�;frontal plane pre-insertion FAST 9.19 ± 2.40�, post-insertion FAST9.75 ± 3.33�; axial plane pre-insertion FAST 17.62 ± 5.03�, post-insertion FAST 18.31 ± 4.94�, Fig. 4b).

4. Discussion

This study is the first to directly investigate if insertion of intra-muscular EMG electrodes into the paraspinal muscles results inreductions in walking speed or amplitude of trunk motion. Unex-

(a) (b)

Fig. 3. Average (a) self-selected locomotor speed, and (b) stride duration atcontrolled speed pre- and post-insertion. Pooled groups, n = 26, error bars = 95%confidence interval, shaded areas = range of equivalence (±minimal detectablechange, MDC).

Fig. 4. Peak-to-peak amplitude of (a) lumbo-pelvic motion, and (b) thoraco-lumbar mbars = 95% confidence interval, shaded areas = range of equivalence (±minimal detectabl

Please cite this article in press as: Armour Smith J, Kulig K. Does insertion of intrmotion?. J Electromyogr Kinesiol (2015), http://dx.doi.org/10.1016/j.jelekin.20

pectedly, self-selected locomotor speed increased following theinsertions. There was a significant decrease in the amplitude oflumbo-pelvic motion in the sagittal plane in response to electrodeinsertions. However, the amplitude of lumbo-pelvic motion infrontal and axial planes, and thoraco-lumbar motion in all planes,was not affected by intramuscular EMG. The levels of anticipatedand actual pain associated with electrode insertion were low inboth groups.

Inferential confidence interval testing demonstrated that theamplitude of sagittal plane motion in the lumbar spine when walk-ing at the controlled speed was significantly smaller followinginsertion of the EMG electrodes. Although the absolute value ofthe decrease in this motion was small (an average reduction ofpeak-to-peak amplitude of 1.11�) it exceeded the minimal detect-able change calculated for this task under these experimental con-ditions. There were different sources of reduced peak-to-peakamplitude in individual participants, with some demonstratingreduced peak flexion, others demonstrating reduced peak exten-sion, and some demonstrating a reduction in both peak flexionand extension. As the duration of the turn at the controlled speedwas not affected by electrode insertion, it is likely that the reduc-tion in sagittal plane motion was due to subject-specific changesin paraspinal agonist and antagonist activity. The fact that changesin locomotor kinematics were evident in sagittal lumbo-pelvicmotion but not in thoraco-lumbar motion may be due to thegreater number of insertions performed in the lumbar region.

Importantly, this study demonstrated that although there weresmall changes in sagittal lumbar motion in response to electrodeinsertion, these changes were the same in individuals with ahistory of recurrent LBP as in healthy individuals. In addition, theindividuals in this study with a history of recurrent LBP did notdemonstrate elevated anticipation of pain or actual pain incomparison with healthy individuals. This is despite the fact thatpersistent LBP is associated with altered cortical processing ofpainful and non-painful sensory stimuli (Wand et al., 2011), centraland peripheral sensitization, and reduced pain pressure threshold,particularly in the area of symptoms (Imamura et al., 2013). The

otion at the controlled speed pre- and post-insertion. Pooled groups, n = 26, errore change, MDC).

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lack of group difference in anticipated and actual pain intensity inthe present study may be due to the fact that the individuals with ahistory of LBP were asymptomatic at the time of the data collectionand had relatively low levels of fear avoidance (Calley et al., 2010).

Self-selected locomotor speed increased following insertion ofthe intramuscular electrodes. Two previous studies investigatingthe effect of electrode insertions in the lower limbs on locomotorspeed have demonstrated both significantly decreased and unal-tered self-selected speed following insertion (Young et al., 2004;Krzak et al., 2013). However, since both of these studies investi-gated children with cerebral palsy they are likely not representa-tive of the response in adults without neurological disorders. AsLBP is normally associated with reduced rather than increasedself-selected locomotor speed (Selles et al., 2001; Lamoth et al.,2006) it is probable that the increase in average self-selected speedevident in this study was a result of an order effect rather thanactual or anticipated discomfort in the insertion area. Prior to thesecond set of self-selected speed trials, the participants had expe-rienced performing the walking circuit at a speed that was fasterthan their comfortable walking pace. This may have resulted inan after-effect during the post-insertion self-selected speed trials.

Numerous studies have demonstrated changes in motor behav-ior in response to acute experimental pain (Farina et al., 2004;Graven-Nielsen and Arendt-Nielsen, 2008; Hodges et al., 2003;Arendt-Nielsen et al., 1995). In this present study however, partic-ipants reported levels of pain both during the insertion of the EMGelectrodes and during the locomotor trials after the insertions thatwere less than the pain typically induced during experimental painprotocols (Moseley et al., 2004; Ervilha et al., 2005 Farina et al.,2004; Arendt-Nielsen et al., 1995). The median VAS value duringlocomotor trials in this study was also less than the pain reportedby participants during fast and slow walking following insertion ofintramuscular electrodes into the gluteal muscles (Semciw et al.,2013). The lower levels of pain experienced in this present studyduring walking may be a result of the slightly lower level of activ-ity in the paraspinal muscles during walking in comparison withthe gluteals (Saunders et al., 2005; Callaghan et al., 1999; Perryand Burnfield, 2010).

Fear of pain and anxiety about future pain may also result inaltered movement strategies and limitation in motor activities(Pincus et al., 2006). Fear of pain has been demonstrated to bemore correlated with guarded movement patterns than actual painintensity (Vlaeyen and Linton, 2000) and anticipation of pain ishighly associated with deficits in locomotor speed in individualswith back pain (Al-Obaidi et al., 2003). However, participants inthis study demonstrated low levels of anticipated pain for boththe insertion of the electrodes and the locomotor trials followinginsertion of electrodes. The VAS scores for anticipated pain werelower than those previously demonstrated during induction ofexperimental low back pain in healthy subjects (Moseley et al.,2004) or during fast walking in individuals with LBP (Al-Obaidiet al., 2003). Individuals who were eligible to take part in this studywere given a full explanation of the intramuscular EMG proceduresprior to volunteering to participate. Therefore, it is likely that indi-viduals with elevated fear of needles or intramuscular EMG meth-odology, who may have experienced greater anticipated pain,chose not to participate. Future studies utilizing intramuscularEMG may benefit from utilizing similar measures of anticipatedand actual pain in order to monitor if their participants may beat greater risk of demonstrated fear-related changes in movementbehavior.

It is important to note that this study investigated the effect ofintramuscular EMG during a sub-maximal task. During bothsteady-state locomotion and walking turns the function of theparaspinal musculature is postural rather than propulsive, andparaspinal activity remains below 20% of the amplitude of maxi-

Please cite this article in press as: Armour Smith J, Kulig K. Does insertion of intrmotion?. J Electromyogr Kinesiol (2015), http://dx.doi.org/10.1016/j.jelekin.20

mum voluntary contraction in these muscles (Saunders et al.,2005). Therefore, it is possible that a larger effect might be evidentduring a motor activity that requires a greater level of paraspinalactivity or a greater range of motion, particularly in the sagittalplane. It should also be noted that in this study, three electrodeinsertions were performed on each participant. This number ofinsertions is consistent with previous studies utilizing intramuscu-lar EMG methodology to investigate trunk control (MacDonaldet al., 2009; Beneck et al., 2013). However, more significant effectsmay also be evident in response to a larger number of electrodeinsertions. In three participants, one of the electrode insertionswas repeated due to the electrode wires being dislodged duringremoval of the inserting needle (n = 2) and poor electrode place-ment (n = 1). Electrode re-insertion did not have a systematic effecton actual pain experienced during the insertions and locomotor tri-als, or on locomotor kinematics in these three individuals.

The findings from this study indicate that other than a small butsystematic change in sagittal plane lumbo-pelvic motion, trunkmotion is not affected by insertion of intramuscular EMG elec-trodes Therefore this is an appropriate method for investigatingtrunk postural control in both individuals with a history of LBPand healthy controls. Future research is needed to clarify if inser-tion of intramuscular EMG electrodes results in more limited sag-ittal plane motion in motor tasks that require greater amplitude ofmotion or higher levels of paraspinal activity than the walking turnin the present study.

Conflict of interest

The authors declare that they have no conflict of interest.

Acknowledgements

The authors would like to thank Lucinda Baker Ph.D., P.T., forher contribution to the design and execution of this project.

This research was supported by a Grant from the OrthopaedicSection of the American Physical Therapy Association, a StudentGrant-in-Aid award from the American Society of Biomechanics,and by the Division of Biokinesiology and Physical Therapy at theUniversity of Southern California.

References

Aadahl M, Jorgensen T. Validation of a new self-report instrument for measuringphysical activity. Med Sci Sports Exerc 2003;35(7):1196–202.

Al-Obaidi SM, Al-Zoabi B, Al-Shuwaie N, Al-Zaabie N, Nelson RM. The influence ofpain and pain-related fear and disability beliefs on walking velocity in chroniclow back pain. Int J Rehabil Res 2003;26(2):101–8.

Angeloni C, Riley P, Krebs D. Frequency content of whole body gait kinematic data.IEEE Trans Rehab Eng 1994;2(1):40–6.

Arendt-Nielsen L, Graven-Nielsen T, Svarrer H, Svensson P. The influence of lowback pain on muscle activity and coordination during gait: a clinical andexperimental study. Pain 1995;64(2):231–40.

Beneck GJ, Baker LL, Kulig K. Spectral analysis of EMG using intramuscularelectrodes reveals non-linear fatigability characteristics in persons withchronic low back pain. J Electromyogr Kinesiol 2013;23(1):70–7.

Callaghan JP, Patla AE, McGill SM. Low back three-dimensional joint forces,kinematics and kinetics during walking. Clin Biomech 1999;14:203–16.

Calley DQ, Jackson S, Collins H, George SZ. Identifying patient fear-avoidance beliefsby physical therapists managing patients with low back pain. J Orthop SportsPhys Ther 2010;40(12):774–83.

Carlsson AM. Assessment of chronic pain. I. Aspects of the reliability and validity ofthe visual analogue scale. Pain 1983;16(1):87–101.

Ervilha UF, Farina D, Arendt-Nielsen L, Graven-Nielsen T. Experimental muscle painchanges motor control strategies in dynamic contractions. Exp Brain Res2005;164(2):215–24.

Farina D, Arendt-Nielsen L, Merletti R, Graven-Nielsen T. Effect of experimentalmuscle pain on motor unit firing rate and conduction velocity. J Neurophysiol2004;91(3):1250–9.

George SZ, Valencia C, Beneciuk JM. A psychometric investigation of fear-avoidancemodel measures in patients with chronic low back pain. J Orthop Sports PhysTher 2010;40(4):197–205.

amuscular electromyographic electrodes alter motor behavior during loco-15.01.003

J. Armour Smith, K. Kulig / Journal of Electromyography and Kinesiology xxx (2015) xxx–xxx 7

Graven-Nielsen T, Arendt-Nielsen L. Impact of clinical and experimental pain onmuscle strength and activity. Curr Rheumatol Rep 2008;10(6):475–81.

Hall L, Tsao H, MacDonald D, Coppieters M, Hodges PW. Immediate effects of co-contraction training on motor control of the trunk muscles in people withrecurrent low back pain. J Electromyogr Kinesiol 2009;19(5):763–73.

Hodges PW, Moseley GL, Gabrielsson A, Gandevia SC. Experimental muscle painchanges feedforward postural responses of the trunk muscles. Exp Brain Res2003;151(2):262–71.

Imamura M, Chen J, Matsubayashi SR, Targino RA, Alfieri FM, Bueno DK, et al.Changes in pressure pain threshold in patients with chronic nonspecific lowback pain. Spine 2013;38(24):2098–107.

Jacobson W, Gabel R. Insertion of fine-wire electrodes does not alter EMG patternsin normal adults. Gait Posture 1995;3:59–63.

King MT. A point of minimal important difference (MID): a critique of terminologyand methods. Expert Rev Pharmacoecon Outcomes Res 2011;11(2):171–84.

Krzak JJ, Corcos DM, Graf A, Smith P, Harris GF. Effect of fine wire electrode insertionon gait patterns in children with hemiplegic cerebral palsy. Gait Posture2013;37(2):251–7.

Lamoth CJC, Daffertshofer A, Meijer O, Moseley GL, Wuisman P, Beek P. Effects ofexperimentally induced pain and fear of pain on trunk coordination and backmuscle activity during walking. Clin Biomech 2004;19(6):551–63.

Lamoth CJC, Daffertshofer A, Meijer O, Moseley GL, Wuisman P, Beek P. Effects ofchronic low back pain on trunk coordination and back muscle activity duringwalking: changes in motor control. Eur Spine J 2006;15(1):23–40.

Lee LJ, Coppieters MW, Hodges PW. Anticipatory postural adjustments to armmovement reveal complex control of paraspinal muscles in the thorax. JElectromyogr Kinesiol 2009;19(1):46–54.

MacDonald D, Moseley GL, Hodges PW. Why do some patients keep hurting theirback? Evidence of ongoing back muscle dysfunction during remission fromrecurrent back pain. Pain 2009;142(3):183–8.

Moe-Nilssen R, Ljunggren AE, Torebjörk E. Dynamic adjustments of walkingbehavior dependent on noxious input in experimental low back pain. Pain1999;83(3):477–85.

Moseley GL, Nicholas MK, Hodges PW. Does anticipation of back pain predispose toback trouble? Brain 2004;27(Pt 10):2339–47.

Perry J, Burnfield JM. Gait analysis. Normal and pathological function, 2nd ed.,Thorofare: SLACK Incorporated; 2010.

Pincus T, Vogel S, Burton AK, Santos R, Field AP. Fear avoidance and prognosis inback pain: a systematic review and synthesis of current evidence. ArthritisRheum 2006;54(12):3999–4010.

Popovich Jr JM, Kulig K. Lumbopelvic landing kinematics and EMG in women withcontrasting hip strength. Med Sci Sports Exerc 2012;44(1):146–53.

Saunders SW, Schache A, Rath D, Hodges PW. Changes in three dimensional lumbo-pelvic kinematics and trunk muscle activity with speed and mode oflocomotion. Clin Biomech 2005;20(8):784–93.

Schache AG, Blanch P, Rath D, Wrigley T, Bennell K. Three-dimensional angularkinematics of the lumbar spine and pelvis during running. Hum Mov Sci2002;21(2):273–93.

Selles RW, Wagenaar RC, Smith TH, Wuisman PI. Disorders in trunk rotation duringwalking in patients with low back pain: a dynamical systems approach. ClinBiomech 2001;16(3):175–81.

Semciw AI, Pizzari T, Green RA. Technical application and the level of discomfortassociated with intramuscular electromyographic investigation into gluteusminimus and medius. Gait Posture 2013;38(1):157–60.

Stanton TR, Latimer J, Maher CG, Hancock MJ. How do we define the condition‘‘recurrent low back pain?’’ A systematic review. Eur Spine J 2009;19(4):533–9.

Please cite this article in press as: Armour Smith J, Kulig K. Does insertion of intrmotion?. J Electromyogr Kinesiol (2015), http://dx.doi.org/10.1016/j.jelekin.20

Stegner BL, Bostrom AG, Greenfield TK. Equivalence testing for use in psychosocialand services research: an introduction with examples. Eval Program Plan1996;19(3):193–8.

Taylor MJD, Dabnichki P, Strike SC. A three-dimensional biomechanical comparisonbetween turning strategies during the stance phase of walking. Hum Mov Sci2005;24(4):558–73.

Tryon WW. Evaluating statistical difference, equivalence, and indeterminacy usinginferential confidence intervals: an integrated alternative method of conductingnull hypothesis statistical tests. Psychol Methods 2001;6(4):371–86.

Tsao H, Danneels LA, Hodges PW. Smudging the motor brain in young adults withrecurrent low back pain. Spine 2011;36(21):1721–7.

Vlaeyen JW, Linton SJ. Fear-avoidance and its consequences in chronicmusculoskeletal pain: a state of the art. Pain 2000;85(3):317–32.

Wand BM, Parkitny L, O’Connell NE, Luomajoki H, McAuley JH, Thacker M, et al.Cortical changes in chronic low back pain: current state of the art andimplications for clinical practice. Manual Ther 2011;16(1):15–20.

Young CC, Rose SE, Biden EN, Wyatt MP, Sutherland DH. The effect of surface andinternal electrodes on the gait of children with cerebral palsy, spastic diplegictype. J Orthop Res 2004;7(5):732–7.

Jo Armour Smith is a post-doctoral fellow in theDivision of Biokinesiology and Physical Therapy atthe University of Southern California. She receivedher B.Sc. in Physiotherapy from the University ofLondon (2001), Masters degree in Manual Therapyfrom the University of Western Australia (2007), andPhD in Biokinesiology from the University of South-ern California (2014). Her research investigates pos-tural control of the trunk and how it is modulated inresponse to musculoskeletal pain, ageing, and skilltraining.

Kornelia Kulig, PhD, PT, FAPTA, FMAAOMPT is aProfessor of Biokinesiology and Orthopedic Surgeryand a Co-Director of the Musculoskeletal Biome-chanics Research Laboratory at the University ofSouthern California. She received her B.Sc. and M.Sc.in Physical Therapy (1976) and her Ph.D. in Biome-chanics (1982) from the Academy of Physical Edu-cation Wroclaw, Poland. From 1982 to 1983, she wasa post-doctoral fellow in Biomechanics of Sport, atthe University of Iowa. Her research explores tissuemorphology, biomechanics, physiology, and pathol-ogy in relation to degenerative processes in connec-tive tissues and accompanying muscle activation,kinematic and kinetic movement strategies andrelated signs, symptoms, and loss of function.

amuscular electromyographic electrodes alter motor behavior during loco-15.01.003