Immediate improvements in activation amplitude levels of the deep abdominal muscle following a sacroiliac joint manipulation during rapid upper limb movement

Accepted Manuscript Immediate improvements in activation amplitude levels of the deep abdominal muscle following a sacroiliac joint manipulation during rapid upper limb movement Alexandre Wesley Carvalho Barbosa , PT, MSc, PhD Adriana Maria Silva , Angélica Fátima Silva , Fábio Luiz Mendonça Martins , PT, MSc, PhD Michelle Cristina Sales Almeida Barbosa , PT PII:

S1360-8592(14)00084-9

DOI:

10.1016/j.jbmt.2014.05.012

Reference:

YJBMT 1140

To appear in:

Journal of Bodywork & Movement Therapies

Received Date: 21 November 2013 Revised Date:

6 May 2014

Accepted Date: 26 May 2014

Please cite this article as: Barbosa, A.W.C., Silva, A.M., Silva, A.F., Martins, F.L.M., Almeida Barbosa, M.C.S., Immediate improvements in activation amplitude levels of the deep abdominal muscle following a sacroiliac joint manipulation during rapid upper limb movement, Journal of Bodywork & Movement Therapies (2014), doi: 10.1016/j.jbmt.2014.05.012. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Immediate improvements in activation amplitude levels of the deep abdominal muscle following a sacroiliac joint manipulation during rapid upper limb movement

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Alexandre Wesley Carvalho Barbosa, PT, MSc, PhDa,*, Adriana Maria Silvaa, Angélica Fátima Silvaa, Fábio Luiz Mendonça Martins, PT, MSc, PhDa, Michelle

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Cristina Sales Almeida Barbosa, PTa

a

Valleys, Minas Gerais, Brazil

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Department of Physiotherapy, Federal University of Jequitinhonha and Mucuri

Department of Physiotherapy - Federal University of Jequitinhonha and Mucuri Valleys. Address: Campus JK - Diamantina - MG - MGT 367 Road - Km 583, nº

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5000 - Alto da Jacuba.

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*Correspondent author at: Department of Physiotherapy - Campus JK Diamantina - MG - MGT 367 Road - Km 583, nº 5000 - Alto da Jacuba.

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Telephone: +55 38 3531 9008. Fax: +55 38 3532 1200. E-mail addresses: [email protected], [email protected]

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Abstract Objective: To assess the immediate effects on the electrical activity of the transversus abdominis/internal oblique (TrA/IO) muscle during rapid voluntary

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upper limb movements before and after a sacroiliac joint (SIJ) manipulation. Methods: Twenty healthy subjects who had innominate fixation, assessed by standing flexion test, were recruited. All subjects were submitted to SIJ

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manipulation and the TrA/IO muscles were evaluated bilaterally, before and after the procedure, through surface electromyography while ten random

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rapid upper limb flexions or abductions were performed. Normality was accepted, and the paired t-test was used to determine data differences (p<0.05). The correlations were calculated using Pearson correlation coefficient. Results: All subjects presented an increase of SIJ mobility after

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manipulation (negative standing flexion test). Significant differences in muscle activation were noted to ipsi- and contralateral TrA/IO recruitment, prior to (A1) and after (A2) the manipulation. The A2 data were statistically

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greater than those in the A1. The Pearson coefficient revealed a strong correlation between the TrA/IO side and the increase in muscle activation

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amplitude level. Also, the data showed a moderate to strong correlation between this last variable and the moments of evaluation. Conclusion: The SIJ manipulation immediately improved the electrical activity of the TrA/IO muscle during rapid voluntary upper limb movements, suggesting improved segment stability and an increment to the afferent stimuli in order to affect the motor response. Key words: Manipulation, Electromyography, Sacroiliac joint, Pelvis

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Introduction The sacroiliac joints (SIJ) are richly innervated by nociceptors and

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proprioceptors, and these joints are the primary source of low-back pain (LBP) episodes (approximately 40% of cases worldwide) (Cusi 2010). The SIJ are also related to the persistent causes of LBP, and lesions in these joints might cause

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biomechanical changes with different pain patterns due to each joint’s

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complex structure and innervation (Barbosa et al. 2013).

The SIJ are also known to be vulnerable to restrictions due to the interaction of descending (e.g. body weight) and ascending (e.g. ground reaction) forces which may contribute to the development of altered joint

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mobility. Asymptomatic individuals may present SIJ mobility restriction and, although such alterations might initially be painless, later segmental muscle adaptations could lead to biomechanical compensations of the surrounding

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soft tissues, overloading other structures and also contributing to the installation and maintenance of a SIJ dysfunction (Grassi et al. 2011).

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Studies have focused on the importance of the gluteus medius and

maximus muscles for motor control and lumbopelvic region stability. These muscles are implicated in musculoskeletal disorders, including LBP and lower limb injuries (Niemuth et al. 2005; Barton et al. 2013). The muscles surrounding the abdominal cavity have been found to play an important role in controlling spinal stability (Sjödahl et al. 2009; Ferreira et al. 2007). An earlier study reported spinal manipulative therapy as a way to produce an

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ACCEPTED MANUSCRIPT inhibitory reflex response that might involve a decrease of motoneuron activity, which in turn may reduce hypertonicity (Dishman et al. 2002). Some researchers have reported the physiologic or functional outcomes of SIJ manipulation, specially high-velocity and low-amplitude thrust (HVLAT)

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techniques, which represent one of the intervention strategies for altered joint motion treatment, also including reduced muscle inhibition, improved periarticular muscle performance, improved gait symmetry, and increased

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range of motion (Orakifar et al. 2012; Barbosa et al. 2013; Cusi 2010; Grassi et

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al. 2011).

Surface electromyography (sEMG) is proposed to give information about muscle activation amplitude levels and insight into the possible mechanisms of the spinal manipulation technique (Lehman 2012). The sEMG has been also used to determine whether dysfunctional or altered motor control patterns

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occur in individuals with musculoskeletal dysfunction (Lehman 2012), contributing in both research and clinical applications to non-invasive

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neuromuscular assessment in different fields such as sport science, neurophysiology, and rehabilitation (Ferreira et al. 2007).

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Various abdominal (rectus, obliques, and transverse abdominal) and

lumbar muscle (such as multifidus) activities have been measured through sEMG (Sjödahl et al. 2009; Rainoldi et al. 2004; Marshall & Murphy 2010) during fast voluntary upper and lower limb movements, especially the transverse abdominis, a deep abdominal muscle involved in trunk control and a contributor to anticipatory postural adjustment for segmental lumbar and pelvic region control during focal movements (Hodges & Richardson 1996).

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ACCEPTED MANUSCRIPT The fast voluntary upper and lower limb movements have been utilised to perturb the trunk equilibrium. This task has been suggested to provide a model to evaluate the effect of spinal manipulation as it provides a measure of the preplanned strategy used by the central nervous system to control the

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trunk muscles (Marshall & Murphy 2010). Also, deficits in abdominal muscle control have been argued to be associated with LBP persistence and chronicity. Reduced or delayed activity is therefore likely to have mechanical

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consequences to the posture and, ultimately, to the subject’s health (Hall et al. 2009; Hodges et al. 2003). The current literature about the role of the

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deep abdominal muscles is linked to temporal analysis, emphasising the anticipatory adjustment and searching for better clinical interventions to solve the delay between the left and right muscles, providing balance to the lumbar and pelvic segment. In reviewing the evidence, the authors did not

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find any reference including the analysis of the signal amplitude level during the trunk equilibrium perturbation or any association to a manipulative procedure, and how this procedure may affect the sEMG signal. This approach

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seems to be important once the muscle amplitude level of activation provides

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information about the force contribution of individual muscles as well as groups of muscles (De Luca 1997), establishing a quantitative relationship between the balance of the studied segment and the surrounding muscle activity.

The aim of the current study is to use SIJ manipulation to observe the immediate

effects

on

the

electrical

activity

of

the

transversus

abdominis/internal oblique (TrA/IO) muscle during rapid voluntary upper limb movements. The hypothesis is that SIJ manipulation may lead to better pelvis

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ACCEPTED MANUSCRIPT and TrA/OI muscle positioning by stabilising the segment, providing afferent stimuli and affecting the motor response, recorded through the sEMG. The muscle response will provide evidence to suggest (or not) the application of

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SIJ manipulation as a tool to affect the lumbar and pelvic segment balance.

Methods Participants

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A total of 42 subjects were screened and 22 did not meet the inclusion

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criteria and were thus excluded. Twenty healthy adult subjects participated in this study, all of whom were right shoulder dominant and were students from the Federal University of Jequitinhonha and Mucuri Valleys in Brazil (22.67±2.64 years of age; IMC=22.75±2.09 kg/m2). The subjects were recruited through public call and during 30 days they were selected by

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physiotherapeutic assessment to exclude hip bone rotation (Van Dillen et al. 2007), leg length discrepancy, pregnancy, diagnosis of ankylosing spondylitis

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and shoulder impingement, presence of neurological signs such as anesthesia, and absence of deep tendon reflexes (Cibulka, Delitto & Koldehoff 1988). The

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inclusion criterion was having a positive standing flexion test (all subjects were retested after the intervention procedure) that presented moderate intra examiner reliability according to Vincent-Smith and Gibbons (1999), although these authors also stated that the reliability of this test as an indicator of SIJ dysfunction still remains questionable. This test determines the side of altered SIJ motion and if there is innominate asymmetry characterised by anterior or posterior innominate restriction (Tong et al. 2006). A movement restriction and an innominate asymmetry are thought to

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ACCEPTED MANUSCRIPT contribute to musculoskeletal pathology in the lumbar, pelvic, and lower limb regions (as leg length discrepancy, excessive lordosis, and scoliosis) (Krawiec et al. 2003). The test was performed by a single, trained and experienced

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therapist. The Federal University of Jequitinhona and Mucuri Valleys’ ethics committee for human investigation approved the procedures employed in the

informed consent prior to participation.

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Data recording and postural task

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study (protocol number 502.230), and all of the subjects gave their written

A biological signal acquisition module with four analogue channels was used (MIOTEC, Biomedical Equipments, Porto Alegre, RS, Brazil). The conversion of analogue to digital signals was performed by an A/D board with

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14-bit resolution input range, sampling frequency of 2 kHz, common rejection module greater than 100 dB, signal noise ratio less than 03 µV RMS, and impedance of 109 ohms. The sEMG signals were recorded by root mean square

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in µV with surface MEDITRACE Ag/AgCl electrodes with a diameter of 2 cm and

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centre to centre distance of 2 cm, applied in a transverse orientation parallel to the underlying fibres on a muscle site representing the combined activity of the TrA/IO (approximately 2 cm medial and 2 cm inferior to the anterior superior iliac spine on each side of the body). The validity and reliability of this site for representing the onset response of the deep abdominals has previously been reported (Marshall & Murphy 2003; Marshall & Murphy 2010; Massé-Alarie et al. 2012). A reference electrode was placed on the left lateral epicondyle. Prior to fixation of the electrodes, the skin was cleaned with 70%

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ACCEPTED MANUSCRIPT alcohol to eliminate residual fat, followed by exfoliation using a specific type of sandpaper for skin and a second cleaning with alcohol. sEMG signals were amplified and filtered (Butterworth fourth order; 20-450 Hz bandpass filter). All sEMG procedures were conducted according to the Non-Invasive

Kinesiology (ISEK) recommendations.

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Assessment of Muscles (SENIAM) International Society of Electrophysiology and

Each subject was required to stand in a relaxed position with their feet

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placed shoulder-width apart, and both arms held in a relaxed position by their

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sides. Ten trials of right shoulder random flexion (a 1) or abduction (Figure 2) were recorded (before the trials, we used an online randomizer tool for each subject - http://stattrek.com/statistics/random-number-generator.aspx) and each repetition was performed as fast as possible from the relaxed vertical position along the trunk in reaction to two different auditory tones (flexion

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and abduction). The shoulder with full-extended elbow had to be flexed to 90°. This created internal perturbations to the trunk and required postural

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adjustments. A time period of 5 seconds was allowed between each trial (Marshall & Murphy 2010; Marshall & Murphy 2006; Tsao et al. 2008). One trial

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consisted of the deltoid onset until the end of muscle activity. These times were visually determined. Visual identification has been shown to be reliable and is preferred to computer-based methods (Hodges & Bui 1996). The trials’ mean were used for comparisons. (figure 1 a and b) (figure 2 a and b)

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ACCEPTED MANUSCRIPT The activation amplitude levels of the ipsilateral (iTrA/IO) and contralateral (cTrA/IO) abdominal muscles for each shoulder movement were the basis of the analysis. The sEMG data were normalised to the three highest peaks to analyse the amplitude levels of activation. Normalising to the peak

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or mean amplitude during the activity of interest has been shown to decrease the variability between individuals compared to using raw sEMG data or when normalising to maximum voluntary isometric contractions (Halaki & Ginn

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2012).

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Intervention

With SIJ asymmetry and its lack of motion confirmed in either anterior or posterior innominate rotation, an HVLAT was applied to the joint in the following manner: (1) the subject was placed in prone position on a low

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treatment table with the hip and knee flexed to 90° (the therapist helped to maintain the position), (2) the contact was made with the therapist’s hands on the SIJ region (both sacral and iliac sides). After reduction of tissue slack

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and joint play, a HVLAT technique was applied once during the subject’s deep exhalation (Figure 3). The standing flexion test and the sEMG data recording

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during the postural task were performed again. (figure 3 ABC)

Data analysis

All statistical analyses were performed using BIOESTAT software (Version 5.0, Belém, PA, Brazil). The G-Power software (Franz Faul, Univesitat Kiel, Germany) was also used to calculate the effect size and the actual

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ACCEPTED MANUSCRIPT sample power, using the coefficient of determination (McCrum-Gardner 2010). The Shapiro-Wilk test was used to test the Gaussian distribution of the variables studied. As normality was accepted, the paired t-test was used to determine whether the differences between the samples were significant at

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the p<0.05 level (CI=95%) and correlations were calculated using Pearson correlation coefficient, assuming 0.8 to 1.0 as a very strong relationship, 0.6 to 0.8 as a strong relationship, 0.4 to 0.6 as a moderate relationship, 0.2 to

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0.4 as a weak relationship, and 0.0 to 0.2 as a weak or no relationship. Sample size calculations, based on power analysis (0.9574) and effect size

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(0.5967), revealed that the sample was larger than necessary to detect changes in the measures under study.

Results

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All subjects presented an increase of SIJ mobility after HVLAT (negative standing flexion test). The mean baselines of the sEMG activity were 1.89±0.23 µV to deltoid, 4.14±1.86 µV to iTrA/IO, and 4.95±2.02 µV to

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cTrA/IO. After the current normalisation, the paired t-test revealed

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significant differences in muscle activation amplitude levels. Figure 4 shows the results of iTrA/IO and cTrA/IO recruitment, prior to (A1) and after (A2) the HVLAT. The A2 data are statistically greater (iTrA/IO: A1=39.73±10.64%; A2=50.79±14.22%; with p=0.0037 and CI-95%=-12.6543 to -0.7771. cTrA/IO: A1= 46.21±10.96%; A2=51.00±7.28%, with p=0.0143 and CI-95%= -10.0921 to 1.7857) than those of the A1. (Figure 4)

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ACCEPTED MANUSCRIPT The Pearson coefficient revealed a strong correlation between the TrA/IO side and the increase in muscle activation amplitude level. Also, the data showed a moderate to strong correlation between this last variable and

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the moments of evaluation (Table 1). (Table 1)

Discussion

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The current study showed increased electromyographic data for both

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sides after the HVLAT, with no statistical differences between cTrA/IO and iTrA/IO before and after the technique, suggesting balance in both assessment moments. A strong correlation between the same side in different moments of assessment (iA1-iA2 and cA1-cA2) was noticed, suggesting a linear behaviour for both sides when the electrical activity was increased. The

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results also showed moderate to strong correlation between muscle side activity in both A1 and A2 and considering the HVLAT was applied once to the

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side of decreased mobility, this balanced and linear effect in an unbalanced area suggests not only local changes, but some central neural integration

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within motor neuronal pools (Pickar 2002; Lederman 1997), possibly eliciting changes in efferent somatomotor activity (Pickar 2002). A developed hypothesis is that the rapid joint separation due to a

HVLAT procedure would stimulate a type IV joint proprioceptor response and a concomitant activation of the muscles in the target area (Wyke 1985). Other studies showed strong electromyographic responses after a manipulation applied to the SIJ in muscles on the treatment side of the back and in muscles located close to the spine on the opposite side (Herzog et al. 1995; Herzog et 11

ACCEPTED MANUSCRIPT al. 1999). The rapid limb movement has been evaluated extensively in the postural response of the trunk muscles. In this task trunk, muscle activity is initiated prior to movement to prepare the spine for the perturbation from limb movement. Notably, activity of TrA, the deepest abdominal muscle, has

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been widely assessed in this task (Aruin & Latash 1995; Hodges & Richardson 1997; Hall et al. 2009; Massé-Alarie et al. 2012). The effect of pre-activation of the trunk muscles stabilises the spine prior to loading and prevents the

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shear and compressive forces associated with vertebral loading and movement

(Marshall & Murphy 2003).

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that are responsible for damage and degeneration of invertebral discs

Indeed, the joint manipulation seems to provide neurophysiological stimuli to deform articular structures rich in sensory inputs, and should lead to changes in the axoplasmic afferent inflow. These changes in sensory input

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are thought to modify neural integration by directly affecting reflex activity (Pickar 2002; Lederman 1997). As the sensory map is continuously corrected

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by sensory feedback according to proprioceptive priority, given by the influx of the afferent receptors (Barbosa et al. 2013; Zusman 2002), we inferred

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that changes in this afferent inflow brought awareness to the CNS, modifying motor patterns during the proposed activity, increasing sEMG activity in both iTrA/IO and cTrA/IO muscles, with more muscle fibres being activated for the same task. An in vivo study showed that SIJ stiffness was increased by certain muscle activity, thus preventing shear (van Wingerden et al. 2004). The TrA/IO has been hypothesised to be important in maintaining SIJ stability due to their transverse fibre orientation (Snijders et al. 1998; Marshall & Murphy 2006). A study showed a TrA contraction significantly decreasing SIJ laxity

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ACCEPTED MANUSCRIPT (Richardson et al. 2002). Also, using a validated static 3-D simulation model, other authors showed the role of the TrA muscle crossing the SIJ and clamping the sacrum between the coxal bones, suggesting that training the TrA muscles could help to relieve SIJ related pelvic pain (Pel et al. 2008). Developing

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strategies to increase the trunk muscles response could be part of a protocol to treat this region.

Against the current results, a study conducted to examine the effect of

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spinal manipulation on electromyographic activity of the low back indicates

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that manipulation induces an immediate change, usually a reduction, in resting levels in patients with LBP and tight paraspinal muscle bundles (DeVocht et al. 2005), although other studies report increased excitability (Herzog et al. 1999; Keller & Colloca 2000). Previous studies showed the HVLAT could either stimulate or silence mechanosensitive receptive nerve

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endings in paraspinal tissues, including muscles, tendons, ligaments, facet joints, and intervertebral discs (Ferreira et al. 2007; Lehman 2012; Indahl et

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al. 1997; DeVocht et al. 2005). These differences could be explained by the muscles’ variability and techniques used to measure these changes. Also, the

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task is widely different for each study. The lack of standard procedures to measure configures a great challenge to compare the results, but the present study focused on the muscle’s ability to respond and stabilise the trunk during a challenge task (rapid arm movement) involving a HVLAT as the interfering factor to change this response, showing the observed increment after the technique, which suggests greater muscle response of both sides during the co-contraction. A previous study reported the difficulty of using existing data to predict how trunk muscle activity would change during a postural

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ACCEPTED MANUSCRIPT adjustment in association with arm movement (Ferreira et al. 2007). The same study indicates that changes following a mobilization technique were only present in people with LBP, and no changes were identified in healthy control subjects, indicating that the pre-existing status of the trunk muscles

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may determine whether activity is modified by the technique. In addition, the recruitment of the TrA did not change with the mobilization (Ferreira et al. 2007). The present data indicate improvements in TrA/IO muscle activity in

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to the previous condition of the subjects.

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healthy subjects, suggesting changes due to the stimulus magnitude and less

Limitations may be addressed. Despite the use of standardised methods to apply the sEMG, the technique allows the cross talk from other surrounding muscles. The sample size calculation was performed to produce statistically significant findings, although the clinical implications of these findings might

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be limited, because they are limited to a young healthy population. Greater participant numbers should be considered during future research. Also,

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caution is needed in applying these findings to clinical practice, especially involving symptomatic patients. The standing flexion test has recognised

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reliability and validity issues. It is important to notice the differences between the normalisation procedure and the data analysis among the studies involving manipulation and sEMG. Moreover, a follow-up study would clarify the long-term effect of the HVLAT in maintaining the increment in muscle activation. These procedures also need to be replicated in an injured population (LBP, leg length differences, SIJ dysfunction, pelvis symptomatic asymmetry) to confirm the findings. There are other muscles that are of equal importance to the trunk during the performance of functional tasks. Further

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ACCEPTED MANUSCRIPT research using sEMG activity across the same task should also consider evaluating sEMG of the quadriceps and other trunk muscles. In conclusion, the results show that SIJ manipulation immediately

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improved the electrical activity of the TrA/IO muscle during rapid voluntary upper limb movements, suggesting improved segment stability and an increment to the afferent stimuli in order to affect the motor response, as seen in the sEMG data. The current results also suggest the application of SIJ

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manipulation as a tool to affect the balance of the lumbar and pelvic

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segment, especially to initiate a program to stabilise the pelvic/low back region and to activate the TrA/IO muscle.

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Tong HC, Heyman OG, Lado DA, Isser MM, 2006. Interexaminer reliability of

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three methods of combining test results to determine side of sacral restriction, sacral base position, and innominate bone position. J Am Osteopath Assoc 106(8): 464-8.

Tsao H, Overs ME, Wu JC, Galea MP, Hodges PW, 2008. Bilateral activation of

1147-52.

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the abdominal muscles induces longer reaction time. Clin Neurophysiol 119(5):

EP

Van Dillen LR, Gombatto SP, Collins DR, Engsberg JR, Sahrmann SA, 2007. symmetry of timing of hip and lumbopelvic rotation motion in 2 different

AC C

subgroups of people with low back pain. Archives of Physical Medicine and Rehabilitation 88(3): 351-360. van Wingerden JP, Vleeming A, Buyruk HM, Raissadat K, 2004. Stabilization of the sacroiliac joint in vivo: verification of muscular contribution to force closure of the pelvis. Eur Spine J 13(3): 199-205. Vincent-Smith B, Gibbons P, 1999. Inter-examiner and intra-examiner reliability of the standing flexion test. Manual Therapy 4(2): 87-93.

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ACCEPTED MANUSCRIPT Wyke BD, 1985. Articular neurology and manipulative therapy. In: Glasgow EF, editor. Aspects of manipulative therapy. London, Churchill Livingstone: 72-80. Zusman M, 2002. Forebrain-mediated sensitization of central pain pathways:

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‘non-specific’ pain and a new image for manual therapy. Manual Therapy 7:

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80-8.

Figure 1 The rapid upper limb movement - flexion. (a) initial position; (b) final position.

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Figure 2 The rapid upper limb movement - abduction. (a) initial position; (b)

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final position.

Figure 3 High velocity low amplitude technique positioning. (A) sacral hand; (B) Iliac hand; (C) therapist helping to maintain the position.

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Figure 4 Mean peak percentage and standard deviation of surface electromyography

(sEMG)

of

ipsi-

(iTrA/IO)

and

contra-lateral

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(cTrA/IO)transverse abdominis/internal oblique, before (A1) and after (A2)

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HVLAT. Significant differences marked (*p=0.0037; **p=0.0143)

Table 1 Pearson coefficient (r), significance (p) and level of correlation. TrA/IO: transverse abdominal/internal oblique; i: ipsilateral; c: contralateral; A1:

assessment

before

the

intervention;

A2:

r

p

assessment

after

the

intervention. Correlation

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0.6526

0.0018

strong

iA1 x cA1

0.6029

0.0049

strong

iA2 x cA2

0.5449

0.0129

moderate

cA1 x cA2

0.7426

0.0002

strong

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TE D

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iA1 x iA2

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TrA/IO

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