Transcript
Page 1: Spectral analysis of EMG using intramuscular electrodes reveals non-linear fatigability characteristics in persons with chronic low back pain

Journal of Electromyography and Kinesiology 23 (2013) 70–77

Contents lists available at SciVerse ScienceDirect

Journal of Electromyography and Kinesiology

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

Spectral analysis of EMG using intramuscular electrodes reveals non-linearfatigability characteristics in persons with chronic low back pain

George J. Beneck a,⇑, Lucinda L. Baker b, Kornelia Kulig b

a Department of Physical Therapy, California State University Long Beach, Long Beach, CA, USAb Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA, USA

a r t i c l e i n f o

Article history:Received 29 March 2012Received in revised form 22 June 2012Accepted 2 July 2012

Keyword:Muscle fatigueMultifidusLow back painMedian frequency

1050-6411/$ - see front matter � 2012 Elsevier Ltd. Ahttp://dx.doi.org/10.1016/j.jelekin.2012.07.001

⇑ Corresponding author. Address: Department ofCalifornia State University Long Beach, 1250 BellfloweUSA. Tel.: +1 562 985 1974; fax: +1 562 985 4069.

E-mail address: [email protected] (G.J. Beneck).

a b s t r a c t

Greater fatigability across lumbar extensors has been reported in persons with chronic low back pain(LBP), however, extensor atrophy tends to be local to the site of pain. Therefore, specific ultrasoundguided local and remote intramuscular electromyographic recordings were undertaken during an isomet-ric horizontal trunk hold in two carefully matched cohorts; persons with and without LBP. The test wasperformed to self-determined maximal hold time, and the control group held the horizontal positionlonger (P < 0.001). A power spectral analysis was performed to calculate the normalized median fre-quency (NMF) slope for both the first and last 30 s of the fatigue test due to the group difference in holdtimes. There were no significant group differences in NMF slope at the first 30 s of testing (P = 0.650). TheNMF slope for the first and last 30 s was not different in healthy subjects (P = 0.688), but was different inpersons with LBP, illustrated by shallowing of the slope at the last 30 s of the test (P = 0.008). A betweenmuscle comparison in the LBP group showed greater non-linear behavior in the deep multifidus (painfulregion) in contrast to T10 longissimus thoracis (nonpainful region) (P = 0.013). Possible explanations forthese findings are discussed.

� 2012 Elsevier Ltd. All rights reserved.

1. Introduction

Several studies have reported greater fatigability of the lumbarextensors in persons with low back pain (LBP) when compared tohealthy persons (De Luca, 1993; Klein et al., 1991; Mayer et al.,1989; Sung et al., 2009; Tsuboi et al., 1994). Most of these studiesanalyzed electromyographic (EMG) signals of the lumbar extensorsduring a brief, but demanding, fatiguing task, such as a horizontaltrunk hold (Demoulin et al., 2006). To determine fatigability,power spectral indices such as the median frequency slope of theEMG signal were generated and used as an indicator of muscle fa-tigue (Klein et al., 1991; Mayer et al., 1989; Roy et al., 1995; Tsuboiet al., 1994). More importantly, this method allows fatigue to beevaluated during the first minute of a task and across variousmuscles. Most studies of individuals with low back pain examinedfatigability across the lumbar extensors globally, however morpho-logic studies indicate that atrophy of the extensors is near the loca-tion of pain (Barker et al., 2004; Beneck and Kulig, 2012; Hideset al., 1994). It is likely that muscles that are atrophied will alsobe more fatigable. In addition, models of regional lumbar stability,

ll rights reserved.

Physical Therapy, ET 122,r Blvd, Long Beach, CA 90840,

developed to describe the roles of distinct components of the lum-bar extensors (Bergmark, 1989), emphasize the intricacies andfunctional importance of the detailed muscular architecture, i.e.individual extensors, in the low back region.

Muscular contributions to stability of the lumbar spine havebeen modeled classifying the lumbar extensors as participating ineither the global or local muscle systems (Bergmark, 1989). Lackingattachments to the lumbar spine, global muscles transfer forcesfrom the thorax to the pelvis and act as guy wires to control spinalorientation. In contrast, the local muscles have direct attachmentsto the lumbar vertebrae and thus control intervertebral motion byimparting optimal stiffness (Panjabi et al., 1989; Wilke et al.,1995). Of the local lumbar extensors, multifidus is considered tobe an important segmental stabilizer due to its greater physiologi-cal cross-sectional area and thus force generating capacity (Wardet al., 2009). However, evidence of the relative fatigability of thevarious lumbar extensors in persons with low back pain is limited.

Morphologic changes (i.e. atrophy, fat infiltration) of the lumbarextensors in persons with low back pain tends to be more pro-nounced in multifidus then in the remaining lumbar extensors(Beneck and Kulig, 2012; Danneels et al., 2000; Mengiardi et al.,2006). One study prospectively validated these local changes inmultifidus (Hodges et al., 2006). In that study, atrophy localizedto one vertebral segment was identified within days following anexperimentally induced injury to the intervertebral disc. Since

Page 2: Spectral analysis of EMG using intramuscular electrodes reveals non-linear fatigability characteristics in persons with chronic low back pain

Table 1Subject characteristics (mean ± SD).

LBP (n = 14) Controls (n = 14) p-Value

Age (years) 34.0 ± 5.4 32.5 ± 5.8 0.486BMI (kg/m2) 23.8 ± 3.9 24.8 ± 4.1 0.516Height (m) 1.76 ± 0.1 1.74 ± 0.1 0.497Weight (kg) 74.8 ± 18.0 75.6 ± 18.0 0.919Symptom duration (years) 7.7 ± 5.9 N/AOswestry disability index (%) 14.9 ± 6.3* N/APhysical activity scale (METS) 43.5 ± 10.6 51.3 ± 14.6 0.119

Abbreviation: LBP, low back pain; METS, metabolic equivalents.* Minimal disability (Fairbank et al., 1980).

G.J. Beneck et al. / Journal of Electromyography and Kinesiology 23 (2013) 70–77 71

the superficial fibers of multifidus span as many as five vertebralsegments, atrophy isolated to one vertebral segment could onlybe explained by selective atrophy of the deep fibers of multifidus.However, no previous studies have examined the fatigability of thedeep fibers of lumbar multifidus in persons with low back pain.Only one study of persons with low back pain has reported greaterfatigability specific to a region of the lumbar extensors (Sung et al.,2009). In that study, greater fatigability was found only in the low-er thoracic erector spinae in persons with chronic low back pain.

Previous electromyographic fatigue studies of the lumbarextensors used surface electrodes (Cooper et al., 1993; Nicolaisenand Jorgensen, 1985; Roy et al., 1989, 1995; Tsuboi et al., 1994).One of the limitations of using surface electrodes with EMG is thatelectrodes tend to record concurrent muscle activity from neigh-boring muscles (Bouisset and Maton, 1970; Perry et al., 1981;Stokes et al., 2003). More specifically, electrical activity of the deepfibers of the multifidus cannot be distinguished from activity of thesuperficial fibers. This is especially relevant, when a demandingisometric horizontal hold is used as the testing position, when allextensors are activated. Using intramuscular electrodes, electricalactivity of the multifidus can be distinguished from the otherextensors such as longissimus thoracis, and the activity of the deepfibers of multifidus can be distinguished from that of the superfi-cial fibers (Moseley et al., 2002, 2003). Fatigue studies using intra-muscular EMG are limited (Christensen et al., 1995; Davis et al.,1998; Fuglsang-Frederiksen and Rønager, 1988; Moritani et al.,1986; Onishi et al., 2000), with only one study examining multifi-dus fatigue (Arabadzhiev et al., 2008). In contrast to surface EMG,intramuscular recordings have a small detection volume and thusrecord activity from a small number of motor units, and high fre-quency signals are not filtered by the subcutaneous tissues as insurface EMG.

A better understanding of how fatigability varies between thelumbar extensors and how this relationship may change withlow back pain will improve our knowledge of the role of the indi-vidual extensors. A greater understanding of these changes androles will lead to more effective interventions for patients withlow back pain. Therefore, the purpose of this study was to comparethe fatigability of the lumbar extensors in persons with and with-out chronic low back pain, both in the painful and nonpainful re-gions. It was hypothesized that the lumbar extensors would bemore fatigable in persons with chronic low back pain, and thatthe deep fibers of the multifidus would be most fatigable in thoseindividuals with chronic low back pain.

2. Methods

2.1. Subjects

Twenty-eight adults (14 males and 14 females) between theages of 23 and 42 years participated. Fourteen participants with ahistory of chronic low back pain (seven males and seven females)were matched with a group (seven males and seven females) with-out a significant history of low back pain (Table 1). Subjects wererecruited from social networks in the Los Angeles area. Prior tosigning a consent form, all subjects were informed about theexperimental procedure, potential risks and purpose of the study.The study was approved by the Institutional Review Board of theUniversity of Southern California.

Subjects were included in the study only if their pain was uni-lateral and localized to the lower lumbar spine region, between theiliac crest and posterior superior iliac spine. The first onset of painmust have been at least one year prior to the date of testing and thesubject must have had an episode of low back pain within the lastsix months. Pain was minimal or absent for at least 3 days prior to

testing. Control subjects, matched for age (±3 years), sex, size, andactivity level (Table 1), did not have any significant episodes of lowback pain for which they have sought medical or other care in thelast 10 years. Neither the low back pain group nor control groupperformed routine heavy lifting or strengthening exercises for theirlumbar extensors for three months prior to testing.

Subjects completed a medical history questionnaire to identifyof any medical condition that would cause him/her to be excludedfrom the study. Subjects were excluded if they responded affirma-tively to the presence of any of the following: bilateral leg symp-toms, clinical or electrophysiological evidence of polyneuropathy,spinal stenosis, prior low back surgery, structural scoliosis, spond-ylolisthesis, known rheumatic joint disease, urinary or fecal incon-tinence, diabetes mellitus, spinal malignancy, spinal infection,pregnancy, or any condition that the subject identifies that mightsignificantly limit participation in physical activity.

2.2. Physical low back screening

The purpose of the low back screen was to characterize eachsubject’s clinical presentation and to clarify consistency with theinclusion criteria. To characterize each subject’s low back condi-tion, common clinical examination procedures for patients withlow back pain were performed including low back pain history,screening for radicular symptoms or overt signs of nerve compres-sion, and tests for lumbar range-of-motion and clinical stability. Alow back pain examination was conducted to confirm the locationof pain in the lower lumbar spine, i.e. L4–5 or L5-S1. Question-naires were completed to assess the level of disability due to lowback pain (Fairbank et al., 1980) and determine the current activitylevel (Aadahl and Jorgensen, 2003) (Table 1).

2.3. Instrumentation and procedures

The evaluation of fatigability was performed on the deep andsuperficial fibers of the multifidus, and the longissimus thoracismuscle in the thoracic and lumbar regions using intramuscularEMG. Electrical activity of multifidus was recorded from the pain-ful side of individuals with low back pain and the matched side ofthe control subjects using fine-wire bipolar electrodes at the L4spinal level as previously described (Moseley et al., 2002, 2003).The electrodes were inserted with the guidance of ultrasoundimaging (Sonoline Antares, Siemens Medical Solutions USA, Inc.,VFX 13-5 linear transducer).

The subjects were positioned prone over a small pillow whilethe spinal levels to be tested are identified with ultrasonic imaging(Fig. 1a). Three electrodes were inserted at the L4 vertebral leveland one at the T10 vertebral level. The first electrode was insertedapproximately 4 cm lateral to the midline and directed mediallytowards the junction of the spinous process and the lamina to re-cord activity from the deep fibers of multifidus (Fig. 1b). A secondelectrode was inserted also at approximately 4 cm lateral to themidline, but was directed to a depth of 1 cm to record activity from

Page 3: Spectral analysis of EMG using intramuscular electrodes reveals non-linear fatigability characteristics in persons with chronic low back pain

Fig. 1. Axial view of multifidus at the L4 level using ultrasound; (a) osseous anatomy of lamina and spinous process outlined, (b) insertion into deep multifidus, (c) insertioninto superficial multifidus.

72 G.J. Beneck et al. / Journal of Electromyography and Kinesiology 23 (2013) 70–77

the superficial fibers of multifidus (Fig. 1c). Similarly, electrodeswere inserted lateral to multifidus into the longissimus thoracismuscle at the L4 and T10 vertebral levels.

The intramuscular electrodes consisted of a pair of 50-lm nick-el–chromium alloy wires with nylon insulation. The distal 2 mmwere thermally stripped of insulation and bent into a hook to stayin the muscle. The electrodes were preloaded into a 25 gaugehypodermic needle to enable insertion. The skin was cleaned withan alcohol swab prior to insertion. The needle with electrodes wasinserted in the muscle; the needle was removed and the electrodes

Fig. 2. (a) Ultrasonic images of the longitudinal view of multifidus at the electrode insertelectrode placement. (b) Thickening of the deep fibers during an electrically elicited confibers during an electrically elicited contraction.

remained. To secure the electrodes in the muscle, isometric resis-tance was applied to the extensors followed by flexion and exten-sion range of motion of the spine in quadruped. Electrodeplacement was confirmed, before and after the fatigue test, byapplying mild electrical stimulation through the wire at its attach-ment to the preamplifier and observing a contraction of the desiredmuscle through the ultrasound image (Fig. 2). A thickening in thefascicle observed on the computer screen of the ultrasound con-firmed the location of the electrode insertion. A reference electrodewas taped over the spinous process of 7th cervical vertebra.

ion site used to confirm electrode placement. This view was used for confirmation oftraction. (c) Superficial fibers without stimulation. (d) Thickening of the superficial

Page 4: Spectral analysis of EMG using intramuscular electrodes reveals non-linear fatigability characteristics in persons with chronic low back pain

Fig. 4. Median frequency of deep multifidus over the initial 30 s during themodified Sorensen test of a single healthy subject.

G.J. Beneck et al. / Journal of Electromyography and Kinesiology 23 (2013) 70–77 73

During the test procedure, electrical signals were transmittedthrough the wires which were attached using MA-416 discrete pre-amplifiers (Motion Lab Systems Inc., Baton Rouge, LA, USA). Thepreamplifiers have a differential input design to reject commonnoise, CMRR > 100 dB at 65 Hz, gain at 1 kHz � 20 ± 1%, inputimpedance >100 MOhms, and a signal bandwidth of 20–3000 Hz.All EMG signals were pre-amplified and sampled at a rate of1560 Hz. Raw signals were stored on a hard drive for later analyses.

2.4. Fatigue testing procedure

A common clinical and research method of testing isometricback extensor fatigability is the Sorensen or modified Sorensen test(Demoulin et al., 2006). In this study, muscle isometric fatigabilitywas tested with the modified Sorensen test using a Backstrongapparatus (Backstrong International LLC, Brea, CA) The Backstrongapparatus allows for testing an isometric contraction of the lumbarextensors with the trunk held in a neutral posture at six inclinationangles, 15�, 30�, 45�, 60�, 75�, and 90�. Once the electrodes were in-serted, each subject performed a 20-s practice trial at 15�, 45�, 75�and 90� before performing the fatigue test at the 90� inclinationangle holding this position as long as possible (Fig. 3). Ample timewas allowed between trial tests to not induce any perceived fati-gue prior to the experimental test. To ensure that the trunk doesnot move during the test, an inclinometer was taped to the sub-ject’s back and a plumb bob hung from the subject’s neck, posi-tioned just above the surface of a table.

2.5. Data processing and analysis

EMG fatigue test data was imported and saved for processingusing MATLAB 7.2 (The Mathworks, USA) signal processing soft-ware. An analysis of this data determined that 95.5% of the signalpower was below 500 Hz, leaving only 4.5% of the power between

Fig. 3. (a) Modified Sorensen test in the final position. Note the plumb bob belowthe subject’s upper torso which could be seen by both the subject and investigatorto monitor any displacement of the trunk during the test. (b) An inclinometerpositioned across upper torso allowed trunk rotation to be monitored throughoutthe duration of the test.

500 and 780 Hz. A power spectral analysis was performed fromeach second of signal data using a fast Fourier transformation todetermine the median frequency for each second of the first andlast 30 s of the fatigue test. The median frequency values wereplotted over time and regression analysis was used to calculatethe rate of change (slope) of the median frequency. An exampleof a typical median frequency slope of a subject with low back painis shown (Fig. 4). The median frequency slope was then normalizedto the initial median frequency. Normalization was performedsince fine-wire EMG recordings include a larger frequency rangethan surface electrodes and because of the inability to controlinterelectrode distance when using fine-wire electrodes. Normaliz-ing the median frequency slope eliminates the possible influencesof the interelectrode distance on the median frequency slope insurface recordings (Farina et al., 2003).

2.6. Statistical analysis

Data were determined to be normally distributed using the Kol-mogorov–Smirnoff test. Differences in NMF slope for each musclebetween groups and within groups were determined using a2 � 4 ANOVA (group �muscle) with repeated measures. The inde-pendent variable (low back pain) was dichotomous (present or ab-sent) and the dependent variable was NMF slope. A paired t-testwas used to compare the maximal hold time in the test positionbetween groups. Because group differences in the duration of thefatigue test were identified, within group differences in NMF slopefor each muscle comparing the first and last 30 s of the fatigue testwere determined using a 2 � 4 ANOVA (group �muscle) with re-peated measures. Because the purpose of the study was to comparethe fatigability of the lumbar extensors in both the painful andnonpainful regions, simple contrast tests were used to analyzethe paired comparisons, with the T10 longissimus thoracis muscleas the reference for comparison. All statistical analyses were per-formed using SPSS software version 17.0 (SPSS, Chicago, IL) withsignificance levels set at p < 0.05.

3. Results

All subjects were able to complete the test without rotating theirtrunk more than 5� and were able to keep the plumb bob from con-tacting the table for the full duration of the test. The average NMFslope for each of the muscles is shown for the initial 30 s of the fati-gue test (Fig. 5). There were no significant differences in NMF slope

Page 5: Spectral analysis of EMG using intramuscular electrodes reveals non-linear fatigability characteristics in persons with chronic low back pain

Fig. 5. Normalized median frequency slope mean and standard error of the meanfor each muscle for the initial 30 s of the test. Initial median frequency was used fornormalization. There were no significant differences between groups.

Fig. 7. Normalized median frequency slope mean and standard error of the meanfor each muscle for the first and last 30 s of the test in subjects with low back pain.⁄Significant main effects for time, first vs. last 30 s. �Significant simple contrast,deep multifidus vs. T10 longissimus thoracis.

74 G.J. Beneck et al. / Journal of Electromyography and Kinesiology 23 (2013) 70–77

values between the low back pain and control groups (P = 0.650)(Fig. 5). Without significant main effects, no post hoc analyses werewarranted. The maximum hold time was significantly greater in thecontrol group (144.4 ± 41.4 s) compared with the group with lowback pain (87.5 ± 25.5 s) (P < 0.001). Consequently, the EMG datawas analyzed for the full duration of the fatigue test.

There were no significant differences in NMF slope values com-paring the first and last 30 s of the fatigue test in the control groups(P = 0.688) (Fig. 6). However, a comparison of the first and last 30 sof the fatigue test in the low back pain group revealed significantdifferences in NMF slope values (P = 0.008) with a significanttime-by-muscle interaction (P = 0.027). Simple contrasts compar-ing the NMF slope values of the three muscles in the painful regionto the NMF slope values of the T10 longissimus thoracis muscle inthe nonpainful region revealed a significant difference with that ofdeep multifidus (P = 0.013), but not superficial multifidus(P = 0.135) or L4 longissimus thoracis (P = 0.114) (Fig. 7).

4. Discussion

Examination of the full test duration yielded a curvilinearbehavior of the NMF over time, best exemplified by the deepmultifidus of subjects with chronic low back pain. The curvilinearbehavior was characterized by an initial rapid decay of the NMFduring the initial 30 s of the test and approaching nearly no slope

Fig. 6. Normalized median frequency slope mean and standard error of the meanfor each muscle for the first and last30 s of the test in healthy subjects. There wereno significant differences between the two time periods.

for the final 30 s. This type of median frequency decay has not beenreported previously in persons with low back pain, however, thisphenomenon has been reported elsewhere. For example, intramus-cular EMG recordings from feline multifidi (Arabadzhiev et al.,2008) during muscle contractions activated reflexively by localstretching of the supraspinous ligament to produce muscle fatigue.The ligament was loaded in successive trials while comparing theeffect of between trial rest duration. The decrease in median fre-quency was initially linear and remained linear with longer be-tween trial rest periods. Shorter between trial rest periodsresulted in a progressive curvilinear decay of the median frequencywith each successive trial. The authors speculated that the changein the rate of median frequency decay may be due to an accumu-lation of fatigue due to shorter rest intervals.

In humans, this curvilinear behavior was reported in the humantibialis anterior with both voluntary and electrically elicited con-tractions, but only when the contractions were of high intensity(e.g. 80% of maximal voluntary contraction) (Merletti et al.,1990). The intensity range of the Sorensen test is from 40% to52% (Demoulin et al., 2006) of maximal voluntary contractionand therefore would not be expected to elicit this curvilinear re-sponse. However, the loading of the tissues local to the low backpain may have been substantially higher in the persons with lowback pain. In our previous work with the same cohort (Beneckand Kulig, 2012), we found an 18% reduction in muscle volumeat the same site where the EMG recordings were performed. Dueto the isolated region of atrophy, we concluded that this could onlybe explained by atrophy of the shortest fibers of multifidus whichare the deep fibers (Beneck and Kulig, 2012). Most previous studieswhich examined the median frequency decay in persons with lowback pain used intensities less than 80%. Studies which used 80% ofmaximal voluntary contraction did not report this behavior of themedian frequency (Candotti et al., 2008; Elfving et al., 2003; Kleinet al., 1991; Lariviere et al., 2003; Oddsson and De Luca, 2003;Peach and McGill, 1998; Roy et al., 1989, 1995, 1997, 1990). How-ever, the ability to achieve a true maximal voluntary contraction inpersons with low back pain has been questioned in several studies(Candotti et al., 2008; Crossman et al., 2004; Humphrey et al.,2005; Kankaanpaa et al., 1998; Kramer et al., 2005; Oddsson andDe Luca, 2003).Furthermore, each of these studies used surfaceEMG and therefore could not record the signal from the deep mul-tifidus which best exemplified this curvilinear behavior.

The lumbar extensors are a very redundant system which controlboth trunk movements and intervertebral motion. With localized

Page 6: Spectral analysis of EMG using intramuscular electrodes reveals non-linear fatigability characteristics in persons with chronic low back pain

G.J. Beneck et al. / Journal of Electromyography and Kinesiology 23 (2013) 70–77 75

atrophy, it is unclear how the load of the trunk will be distributedbetween the extensors. Load sharing between the extensors hasbeen proposed as a neuromuscular strategy to delay muscle fatiguebetween the extensors (van Dieen et al., 1993). However, the curvi-linear decay of the median frequency demonstrated in previousstudies was only present under the most demanding protocols.Therefore, the data from the current study indicates that the demandon the muscles in the atrophied region was high during the horizon-tal trunk hold. This high demand on the atrophied region may, inpart, explain the much shorter durations of the horizontal trunk holdin the patients with low back pain.

An additional explanation for the curvilinear behavior of themedian frequency decay in the current is as follows. Fast fibersare responsible for much of the high frequency content of theEMG power spectrum (Tesch et al., 1983). During a fatiguing task,the median frequencies of muscles with a high proportion of fastfibers diminish at a higher rate (Hakkinen and Komi, 1986; Komiand Tesch, 1979; Kupa et al., 1995; Moritani et al., 1982) than mus-cles with a higher proportion of slow fibers. In patients with lowback pain, selective atrophy of fast fibers is a frequent finding dur-ing intraoperative biopsies (Fidler et al., 1975; Kalimo et al., 1989;Mattila et al., 1986; Rantanen et al., 1993; Zhu et al., 1989). In thecurrent study, the initial decay in the median frequency in the sub-jects with low back pain may be due to fatigue of the atrophied,more fatigable, fast fibers. During the flattening of the median fre-quency slope, the load during the test may have been carried pri-marily by the reserve of less fatigable, non-atrophied, slow fibers.One study has examined both power spectral changes and fibertype atrophy in patients with and without chronic low back pain(Crossman et al., 2004). No group differences in median frequencyslope or fiber atrophy were reported. However, EMG recordingswere collected with surface electrodes which cannot record theEMG signal from isolated muscles, nor were the biopsy locationsspecific to the site of pain.

The results of the current study do not indicate any group differ-ences in the NMF slope of the lumbar extensors during the first 30 sof the horizontal trunk hold as hypothesized. These results are sim-ilar to several studies which did not report greater fatigability in sub-jects with low back pain (Crossman et al., 2004; Elfving et al., 2003;Kramer et al., 2005; Lariviere et al., 2003). The results of each of thesestudies were explained by the load used to fatigue the extensors. Theload was determined as a percentage of maximum strength. As dis-cussed above, maximum strength measures may not have been truemaximums, thus the load used to fatigue the extensors may havebeen less for the subjects with low back pain in these studies. Thisexplanation would not account for the lack of group differences inthe current study since subjects used their body weight rather thana load normalized to a maximum strength test.

The lack of group differences reported of the initial median fre-quency slope in the current study differs from many of the previousreports (Klein et al., 1991; Mayer et al., 1989; Roy et al., 1989, 1995;Sung et al., 2009; Tsuboi et al., 1994). There are two possible expla-nations for the lack of differences between the current and previousstudies. First, in one study (Roy et al., 1995), the severity of the sub-jects with chronic low back pain appeared greater than that of thecurrent study. Seventy-five percent had a disc herniation and somehad previous back surgery. It is possible that the severity of lowback pain and extent of morphological pathology of the subjectsin the current study was too low to show group differences. Sub-jects with low back pain in the current study were similar in Osw-estry scores and pain duration to two previous studies that also didnot show group differences in fatigability (da Silva et al., 2005; Kan-kaanpaa et al., 1998). Second, several studies did not control foractivity level as part of their inclusion criteria (Mannion and Dolan,1994; Mayer et al., 1989; Roy et al., 1995; Sung et al., 2009; Tsuboiet al., 1994). As a result, differences in fatigability between groups

may have been influenced by the subject’s habitual activity level.If the subjects with low back pain in the previous studies were lessactive, this could explain their greater fatigability, rather than theirback pain alone. For instance, Roy et al. (1989) reported greater fati-gability of the lumbar extensors in a subject population of similarduration (average = 5.2 years) to the current study, but the degreeof disability was not reported and the authors suggested that thegroup with low back pain was less physically active than the controlgroup. Thus, either higher disability or reduced physical activity ofthe group with low back pain may explain the group differences re-ported in that study. One study reported group differences in med-ian frequency slope in subject with a similar activity level.However, the subjects consisted of a very active population, i.e. col-lege rowers with and without low back pain (Klein et al., 1991). Per-haps the homogeneity of an athletic group provided less withingroup variability resulting in a between group difference.

Despite the lack of group differences in the NMF slope, the max-imum hold time was nearly one minute longer in the controlgroup. This is consistent with previous studies which examinedfatigability using hold times in subjects with low back pain (Cross-man et al., 2004; Nicolaisen and Jorgensen, 1985; Nourbakhsh andArab, 2002). However, hold times during the Sorensen test can varyfor reasons other than fatigue of the extensors. In one study, 37.5%of subjects stopped for reasons such as pain in the lower extremi-ties, back pain, or lack of motivation (Ropponen et al., 2005). In thatstudy, those with a history of low back pain had a greater likeli-hood of terminating the test due to back pain or fear of back painexperienced during the test. However, our records did not showthat any of the subjects stopped due to an onset of low back pain.

5. Conclusion

An intramuscular EMG spectral analysis of the lumbar extensorsconducted on persons with chronic unilateral low back pain didnot demonstrate group differences in median frequency slope dur-ing the first 30 s of the test. However, analysis of the full durationof the test revealed a curvilinear decay of the median frequencyonly at the site of pain in persons with low back pain. Such findingsmay, in part, explain group differences in hold times, but also indi-cate that fatigability responses may differ in muscle at the site oflow back pain.

Acknowledgements

Supported by the Health Research Association (HRA) of the Uni-versity of Southern California (HRA Seed grant; project no. 227500)and by the Promotion of Doctoral Studies Scholarship through theFoundation for Physical Therapy.

Appendix A. Supplementary data

Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.jelekin.2012.07.001.

References

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

Arabadzhiev T, Solomonow M, Zhou BH, Dimitrova N, Dimitrov G. Power spectracharacteristics associated with static reflexive activation of the multifidusmuscle in feline models. Eur J Appl Physiol 2008;104:873–83.

Barker KL, Shamley DR, Jackson D. Changes in the cross-sectional area of multifidusand psoas in patients with unilateral back pain: the relationship to pain anddisability. Spine 2004;29:E515–9.

Beneck GJ, Kulig K. Multifidus atrophy is localized and bilateral in active personswith chronic unilateral low back pain. Arch Phys Med Rehabil 2012;93:300–6.

Page 7: Spectral analysis of EMG using intramuscular electrodes reveals non-linear fatigability characteristics in persons with chronic low back pain

76 G.J. Beneck et al. / Journal of Electromyography and Kinesiology 23 (2013) 70–77

Bergmark A. Stability of the lumbar spine. A study in mechanical engineering. ActaOrthop Scand Suppl 1989;230:1–54.

Bouisset S, Maton B. Comparison between surface and intramuscular EMG’s involuntary movements. Electroencephalogr Clin Neurophysiol 1970;29:533.

Candotti CT, Loss JF, Pressi AM, Castro FA, La Torre M, Melo Mde O, et al.Electromyography for assessment of pain in low back muscles. Phys Ther2008;88:1061–7.

Christensen H, Søgaard K, Jensen BR, Finsen L, Sjøgaard G. Intramuscular and surfaceEMG power spectrum from dynamic and static contractions. J ElectromyogrKinesiol 1995;5:27–36.

Cooper RG, Stokes MJ, Sweet C, Taylor RJ, Jayson MI. Increased central drive duringfatiguing contractions of the paraspinal muscles in patients with chronic lowback pain. Spine 1993;18:610–6.

Crossman K, Mahon M, Watson PJ, Oldham JA, Cooper RG. Chronic low back pain-associated paraspinal muscle dysfunction is not the result of a constitutionallydetermined ‘‘adverse’’ fiber-type composition. Spine 2004;29:628–34.

da Silva RA, Arsenault Jr AB, Gravel D, Lariviere C, de Oliveira Jr E, et al. Back musclestrength and fatigue in healthy and chronic low back pain subjects: acomparative study of 3 assessment protocols. Arch Phys Med Rehabil2005;86:722–9.

Danneels LA, Vanderstraeten GG, Cambier DC, Witvrouw EE, De Cuyper HJ. CTimaging of trunk muscles in chronic low back pain patients and healthy controlsubjects. Eur Spine J 2000;9:266–72.

Davis BA, Krivickas LS, Maniar R, Newandee DA, Feinberg JH. The reliability ofmonopolar and bipolar fine-wire electromyographic measurement of musclefatigue. Med Sci Sports Exerc 1998;30:1328–35.

De Luca CJ. Use of the surface EMG signal for performance evaluation of backmuscles. Muscle Nerve 1993;16:210–6.

Demoulin C, Vanderthommen M, Duysens C, Crielaard JM. Spinal muscle evaluationusing the Sorensen test: a critical appraisal of the literature. Joint Bone Spine2006;73:43–50.

Elfving B, Dedering A, Nemeth G. Lumbar muscle fatigue and recovery in patientswith long-term low-back trouble – electromyography and health-relatedfactors. Clin Biomech (Bristol, Avon) 2003;18:619–30.

Fairbank JC, Couper J, Davies JB, O’Brien JP. The Oswestry low back pain disabilityquestionnaire. Physiotherapy 1980;66:271–3.

Farina D, Gazzoni M, Merletti R. Assessment of low back muscle fatigue by surfaceEMG signal analysis: methodological aspects. J Electromyogr Kinesiol2003;13:319–32.

Fidler MW, Jowett RL, Troup JD. Myosin ATPase activity in multifidus muscle fromcases of lumbar spinal derangement. J Bone Joint Surg Br 1975;57:220–7.

Fuglsang-Frederiksen A, Rønager J. The motor unit firing rate and the powerspectrum of EMG in humans. Electroencephalogr Clin Neurophysiol1988;70:68–72.

Hakkinen K, Komi PV. Effects of fatigue and recovery on electromyographic andisometric force- and relaxation-time characteristics of human skeletal muscle.Eur J Appl Physiol Occup Physiol 1986;55:588–96.

Hides JA, Stokes MJ, Saide M, Jull GA, Cooper DH. Evidence of lumbar multifidusmuscle wasting ipsilateral to symptoms in patients with acute/subacute lowback pain. Spine 1994;19:165–72.

Hodges P, Holm AK, Hansson T, Holm S. Rapid atrophy of the lumbar multifidusfollows experimental disc or nerve root injury. Spine 2006;31:2926–33.

Humphrey AR, Nargol AV, Jones AP, Ratcliffe AA, Greenough CG. The value ofelectromyography of the lumbar paraspinal muscles in discriminating betweenchronic-low-back-pain sufferers and normal subjects. Eur Spine J 2005;14:175–84.

Kalimo H, Rantanen J, Viljanen T, Einola S. Lumbar muscles: structure and function.Ann Med 1989;21:353–9.

Kankaanpaa M, Taimela S, Laaksonen D, Hanninen O, Airaksinen O. Back and hipextensor fatigability in chronic low back pain patients and controls. Arch PhysMed Rehabil 1998;79:412–7.

Klein AB, Snyder-Mackler L, Roy SH, DeLuca CJ. Comparison of spinal mobility andisometric trunk extensor forces with electromyographic spectral analysis inidentifying low back pain. Phys Ther 1991;71:445–54.

Komi PV, Tesch P. EMG frequency spectrum, muscle structure, and fatigue duringdynamic contractions in man. Eur J Appl Physiol Occup Physiol 1979;42:41–50.

Kramer M, Ebert V, Kinzl L, Dehner C, Elbel M, Hartwig E. Surface electromyographyof the paravertebral muscles in patients with chronic low back pain. Arch PhysMed Rehabil 2005;86:31–6.

Kupa EJ, Roy SH, Kandarian SC, De Luca CJ. Effects of muscle fiber type and size onEMG median frequency and conduction velocity. J Appl Physiol 1995;79:23–32.

Lariviere C, Arsenault AB, Gravel D, Gagnon D, Loisel P. Surface electromyographyassessment of back muscle intrinsic properties. J Electromyogr Kinesiol2003;13:305–18.

Mannion AF, Dolan P. Electromyographic median frequency changes duringisometric contraction of the back extensors to fatigue. Spine 1994;19:1223–9.

Mattila M, Hurme M, Alaranta H, Paljarvi L, Kalimo H, Falck B, et al. The multifidusmuscle in patients with lumbar disc herniation. A histochemical andmorphometric analysis of intraoperative biopsies. Spine (Phila Pa 1976)1986;11:732–8.

Mayer TG, Kondraske G, Mooney V, Carmichael TW, Butsch R. Lumbar myoelectricspectral analysis for endurance assessment. A comparison of normals withdeconditioned patients. Spine 1989;14:986–91.

Mengiardi B, Schmid MR, Boos N, Pfirrmann CW, Brunner F, Elfering A, et al. Fatcontent of lumbar paraspinal muscles in patients with chronic low back painand in asymptomatic volunteers: quantification with MR spectroscopy.Radiology 2006;240:786–92.

Merletti R, Knaflitz M, De Luca CJ. Myoelectric manifestations of fatigue in voluntaryand electrically elicited contractions. J Appl Physiol 1990;69:1810–20.

Moritani T, Muro M, Nagata A. Intramuscular and surface electromyogram changesduring muscle fatigue. J Appl Physiol 1986;60:1179–85.

Moritani T, Nagata A, Muro M. Electromyographic manifestations of muscularfatigue. Med Sci Sports Exerc 1982;14:198–202.

Moseley GL, Hodges PW, Gandevia SC. Deep and superficial fibers of the lumbarmultifidus muscle are differentially active during voluntary arm movements.Spine 2002;27:E29–F36.

Moseley GL, Hodges PW, Gandevia SC. External perturbation of the trunk instanding humans differentially activates components of the medial backmuscles. J Physiol 2003;547:581–7.

Nicolaisen T, Jorgensen K. Trunk strength, back muscle endurance and low-backtrouble. Scand J Rehabil Med 1985;17:121–7.

Nourbakhsh MR, Arab AM. Relationship between mechanical factors and incidenceof low back pain. J Orthop Sports Phys Ther 2002;32:447–60.

Oddsson LI, De Luca CJ. Activation imbalances in lumbar spine muscles in thepresence of chronic low back pain. J Appl Physiol 2003;94:1410–20.

Onishi H, Yagi R, Akasaka K, Momose K, Ihashi K, Handa Y. Relationship betweenEMG signals and force in human vastus lateralis muscle using multiple bipolarwire electrodes. J Electromyogr Kinesiol 2000;10:59–67.

Panjabi M, Abumi K, Duranceau J, Oxland T. Spinal stability and intersegmentalmuscle forces. A biomechanical model. Spine 1989;14:194–200.

Peach JP, McGill SM. Classification of low back pain with the use of spectralelectromyogram parameters. Spine 1998;23:1117–23.

Perry J, Easterday CS, Antonelli DJ. Surface versus intramuscular electrodes forelectromyography of superficial and deep muscles. Phys Ther 1981;61:7–15.

Rantanen J, Hurme M, Falck B, Alaranta H, Nykvist F, Lehto M, et al. The lumbarmultifidus muscle five years after surgery for a lumbar intervertebral discherniation. Spine (Phila Pa 1976) 1993;18:568–74.

Ropponen A, Gibbons LE, Videman T, Battie MC. Isometric back extension endurancetesting: reasons for test termination. J Orthop Sports Phys Ther 2005;35:437–42.

Roy SH, De Luca CJ, Casavant DA. Lumbar muscle fatigue and chronic lower backpain. Spine 1989;14:992–1001.

Roy SH, De Luca CJ, Emley M, Buijs RJ. Spectral electromyographic assessment ofback muscles in patients with low back pain undergoing rehabilitation. Spine1995;20:38–48.

Roy SH, De Luca CJ, Emley M, Oddsson LI, Buijs RJ, Levins JA, et al. Classification ofback muscle impairment based on the surface electromyographic signal. JRehabil Res Dev 1997;34:405–14.

Roy SH, De Luca CJ, Snyder-Mackler L, Emley MS, Crenshaw RL, Lyons JP. Fatigue,recovery, and low back pain in varsity rowers. Med Sci Sports Exerc1990;22:463–9.

Stokes IA, Henry SM, Single RM. Surface EMG electrodes do not accuratelyrecord from lumbar multifidus muscles. Clin Biomech (Bristol, Avon)2003;18:9–13.

Sung PS, Lammers AR, Danial P. Different parts of erector spinae muscle fatigabilityin subjects with and without low back pain. Spine J 2009;9:115–20.

Tesch PA, Komi PV, Jacobs I, Karlsson J, Viitasalo JT. Influence of lactateaccumulation of EMG frequency spectrum during repeated concentriccontractions. Acta Physiol Scand 1983;119:61–7.

Tsuboi T, Satou T, Egawa K, Izumi Y, Miyazaki M. Spectral analysis ofelectromyogram in lumbar muscles: fatigue induced endurance contraction.Eur J Appl Physiol Occup Physiol 1994;69:361–6.

van Dieen JH, Oude Vrielink HH, Toussaint HM. An investigation into the relevanceof the pattern of temporal activation with respect to erector spinae muscleendurance. Eur J Appl Physiol Occup Physiol 1993;66:70–5.

Ward SR, Kim CW, Eng CM, Gottschalk LJ, Tomiya A, Garfin SR, et al. Architecturalanalysis and intraoperative measurements demonstrate the unique design ofthe multifidus muscle for lumbar spine stability. J Bone Joint Surg Am2009;91:176–85.

Wilke HJ, Wolf S, Claes LE, Arand M, Wiesend A. Stability increase of the lumbarspine with different muscle groups. A biomechanical in vitro study. Spine1995;20:192–8.

Zhu XZ, Parnianpour M, Nordin M, Kahanovitz N. Histochemistry and morphologyof erector spinae muscle in lumbar disc herniation. Spine (Phila Pa 1976)1989;14:391–7.

George J. Beneck is an Associate Professor in theDepartment of Physical Therapy at California StateUniversity Long Beach. He received the B.Sc. in PhysicalTherapy at Temple University (1984), M.Sc. in Biome-chanics at Michigan State University (1991), and Ph.D.in Biokinesiology at the University of Southern Califor-nia (2010). His research examines how spinal motionand paraspinal muscle performance are altered inassociation with spinal disorders, and how variousmanual and exercise interventions alter spinal motionand muscle performance.

Page 8: Spectral analysis of EMG using intramuscular electrodes reveals non-linear fatigability characteristics in persons with chronic low back pain

G.J. Beneck et al. / Journal of Electromyography and Kinesiology 23 (2013) 70–77 77

Lucinda L. Baker is an Associate Professor in the Divi-sion of Biokinesiology and Physical Therapy at theUniversity of Southern California where she is theDirector of the Clinical Electrophysiology Laboratory.She received her B.Sc. (1972), M.Sc. (1977), and Ph.D.(1985) in Physical Therapy at the University of SouthernCalifornia. Her research focus is on the evaluation of thehuman nervous system, specifically assessing thestate of motoneuron and interneuron excitability atthe level of the spinal cord. Dr. Baker teaches inthe areas of electrophysiology, neurophysiology andneuroanatomy.

Kornelia Kulig, PhD, PT, FAPTA, FMAAOMPT is a Pro-fessor of Biokinesiology and Orthopedic Surgery and aCo-Director of the Musculoskeletal BiomechanicsResearch Laboratory at the University of Southern Cal-ifornia. She received her B.Sc. and M.Sc. in PhysicalTherapy (1976) and her Ph.D. in Biomechanics (1982)from the Academy of Physical Education Wroclaw,Poland. From 1982 to 1983, she was a post-doctoralfellow in Biomechanics of Sport, at the University ofIowa. Her research explores tissue morphology, bio-mechanics, physiology, and pathology in relation todegenerative processes in connective tissues and

accompanying muscle activation, kinematic and kinetic movement strategies andrelated signs, symptoms, and loss of function.


Top Related