EMG-pressure Response in the Transverse Abdominis and Multifidus Muscles among Individuals With and Without Chronic Low Back Pain


 Background: Pressure biofeedback unit (PBU) is a non-invasive, low-cost, and widely used device for monitoring, evaluating and training transverse abdominals (TA) and multifidus (MF) muscles of patients with low back pain (LBP). There has been little research on quantifying muscle activity under different pressures. The primary aim of this preliminary study was to explore the response between deep local trunk muscles (TA and MF) and different target pressures of PBU in seated positions. Methods: Twenty-two patients with chronic LBP (cLBP) and 24 age matched healthy individuals were recruited. Electromyography (EMG) signals were recorded from the TA and MF muscles while individuals contract the TA and MF muscles in seated position to achieve PBU pressure value of 50, 60 and 70mmHg in random order. The t-test was used to compare between-group and within-subjects’ effects to examine the effect of different pressure values. Spearman’s correlation analysis was performed in the cLBP group to determine potential correlations. Results: The %MVIC of the TA and MF in the cLBP group were statistically higher than the control group at each pressure value (P＜0.05). The slope of the cLBP subjects was significantly steeper than the healthy control subjects (TA: P=0.01, MF: P＜0.001). During maximal voluntary isometric contraction (MVIC) of TA and MF, compared with pain-free group, cLBP patients showed a significant decrease (P≤0.001). MF MVIC was significantly and moderately negatively correlated with visual analog scale (VAS) (r = -0.48, P=0.024) and Oswestry Disability Index (ODI) (r = -0.59, P=0.004). Conclusions: The study demonstrates the feasibility of using PBU to assess muscle contraction that corresponds with changes of muscle activity as measured by EMG. The use of EMG to quantify the extent of how much the PBU activates muscles may provide important information to clinicians and researchers for patients with LBP.


Background
Low back pain (LBP) is one of the most common and challenging musculoskeletal conditions encountered by health care professionals [1][2][3]. It is the main leading cause of non-fatal health loss for nearly three decades and a major contributor to global disability burden [4]. LBP accounts for the excessive direct (health care) and indirect (lost production and lost household productivity) health costs as well as a major social and economic impact [2,3,5]. Animal experiment [6] and mathematical model of the spine [7] indicated that sequential injuries and deep muscles weakness resulted in spinal instability. The hypothesis of spinal instability is defined as a significant decrease in the capacity of the spinal stabilizing system to maintain the intervertebral neutral zone within the physiological limits [8]. Clinical guidelines based on the meta-analysis and systematic review on the treatment of LBP, strongly recommend motor control stabilization exercises are an effective intervention for LBP [2,[9][10][11], in particular segmental spinal stabilization exercises (SSEs) [12,13]. A systematic review reported that SSEs could reduce the level of pain during acute flare up and the long-term recurrence of chronic LBP (cLBP) [14]. The principle of SSEs is to train the co-contraction pattern of the deep local trunk muscles of the transversus abdominis (TA) and the multifidus muscles (MF). These two muscles are the primary segmental stabilization muscle of the trunk [15,16] which activate in advance of the trunk movement to produce, equilibrium force that counteracts the perturbation force generated during rapid movements of the arms and legs that destabilize the spine [17][18][19].
The quantitative measurement of the function and strength of MF and TA plays a crucial role in assessing muscle activation pattern and clinical effectiveness of SSEs and other interventions. Direct measurements of MF and TA muscles functions often relies on indirect methods of electromyography (EMG), ultrasound imaging or a pressure biofeedback unit (PBU). The gold-standard to measure the activity of the deep local trunk muscles is by fine-wire electromyography [17,18]. However, factors such as pain, discomfort and risk of infection limits its clinical application as routine outcome measure. Surface EMG also has the limitation of cross-talk with other muscles that are in close proximity [20]. High cost and inconvenient hinders the common use of ultrasound imaging in clinical practice. PBU has the potential to be a non-invasive, low-cost and convenient assessment tool to be used in clinical and research setting to objectively quantify TA activation [21]. This device measures the change of pressure (mmHg) that the abdominal wall or low back exerts on the lumbar spine during the voluntarily activation of the TA and MF muscles as they perform dedicated postures [22]. Furthermore, the reproducibility of PBU in measuring TA muscle activity of LBP [23] and healthy [24] individuals have reported to be excellent for intra and inter-examiner reproducibility.
Previous studies suggested that the pretrial baseline pressure was set at 70 mmHg for prone [21,23] position and 40 mmHg for hook-lying supine [22,25,26], side-lying [27] and upright [22,26] positions. However, fewer studies were conducted for seated position. In Australia, 70% of adults sit for more than 8 h per day [28], and the time likely to extend due to the increasing use of social media [29]. Prolonged sitting seems to be unavoidable in our modern daily life, work and study. Training the TA and MF muscles with PBU in the correct sitting position could increase lumbar stability [22,30,31], which might be one of the measures to reduce the occurrence of LBP [31]. Published studies assessed the activity of TA at a specific pressure (40 mmHg  The aims of this study were to compare muscle activities of the TA and MF between individuals with and without cLBP; and to explore the difference between deep local trunk muscles of TA, MF at different target pressures (50, 60 and 70 mmHg) of PBU in the two groups.

Materials And Methods Subjects
Subjects were recruited from the local rehabilitation ward and outpatient department of the hospital.
The inclusion criteria of LBP subjects were as follows: 1) experienced pain in the low back region with or without accompanying buttock pain over the past three months and of sufficient intensity to have limited activities of daily living [23]; 2) pain score range between 3-7 on the visual analogue scale (VAS) [30]; and 3) able to perform the experiment procedure without symptom aggravation. This was to minimize the variability in the level of pain during testing which may increase the variability of the data. Exclusion criteria were: 1) existence of respiratory, orthopaedic, circulatory or neurological conditions; 2) previous surgery to the abdomen or lower back; 3) female participants who were pregnant or suffered from dysmenorrhea; 4) epilepsy or had family history of epilepsy. Age matched healthy individuals were recruited as control.

Ethics
The study protocol was reviewed and approved by the Human Subjects Ethics Sub-committee of the First Affiliated Hospital, Sun Yat-sen University (Approval number: [2017] C-034). All subjects gave written informed consent. The study was conducted in accordance to the Declaration of Helsinki.

Instruments
The Pressure Biofeedback Unit (PBU) (Chattanooga Group Inc., LLC Vista, California, USA) employed in this study is made up of a three-chamber air-filled pressure cell, a catheter and a sphygmomanometer gauge. The pressure cell of the PBU was made from latex-free rubber material, and the unfolded dimensions of the cell were 16.7 × 24.0 cm. The sphygmomanometer has a range between 0 to 200 mmHg and was calibrated at 2 mmHg interval. Movement or change in position causes volume changes in the pressure cells that is recorded on the gauge. Prior to data recording, the pressure cell was first inflated to a pressure of 40 mmHg (orange band) and then closed the valve to stop air leakage [25,26]. To ensure accuracy of the PBU measurements, the device was pretested by loading the biofeedback unit cushion with a static weight of 4 kg for 24 hours. The PBU was only considered adequate if the device lost no more than 0.5 mmHg during the 24-hour period [33].
Surface electromyography A UMI-SE-I system (Shaoxing United Medical Instruments Co., LTD, China) was used to record muscle activity with active electrodes. EMG signals with common mode rejection ratio (110db), bandwidth (15-1000 Hz) and resolution (0.1 µV). Sampling frequency of the EMG system was set at 3000 Hz and stored in the computer for offline analysis [30]. To reduce skin impedance, hair was removed from the measurement sites and the skin deterged with alcohol before electrode placement. Disposable Ag/AgCl surface electrodes were attached to the concerned muscle.
The maximum spacing between the recording electrodes was 2 cm. The locations of the EMG electrodes were determined in accordance to sEMG sensor placement guidelines [34] and published studies [23,32,35]. Electrodes to measure TA activity were placed at the center position 2 cm cephalic to the pubic bone, just lateral to the midline, and parallel to the superior pubic ramus along either side of the course of the underlying muscle fibers [23,32,34,35]. For MF, electrodes were placed at the level of the L5 spinous process along the line joining the posterosuperior iliac spine (PSIS) and L1-L2 vertebral interspace [34,35]. The maximal voluntary isometric contraction (MVIC) was measured to determine the level of voluntary contractions during testing. Each subject was asked to perform maximum contraction of each muscle and hold for 5 seconds. MVIC was repeated 3 times and the highest value was selected [34,34]. The average EMG amplitude (AEMG) of 3 replicate trials was used in the analysis after normalization to %MVIC [20,34], which was calculated for the selected muscles using the formula:

Experimental Procedures
Demographic information and background clinical information were first collected. All participants then received basic information about the anatomy, biomechanics and functions of the TA and MF muscles. All participants were instructed to fast for at least two hours prior to testing, to empty their bladder in advance of the assessment, and to avoid performing any type of abdominal exercises prior to the test [20,21]. The methods of PBU tests to be carried out were described in Table 1. They were performed in random order by selecting a single card with three cards marked with either 1 (50 mmHg), 2 (60 mmHg), or 3 (70 mmHg). The examiner provided verbal instructions throughout the test. All subjects in the pain-free group selected the muscles on the right side. Subjects in the cLBP group chose the more painful side as target muscles. Three trials were conducted for each target pressure and the averaged values were used for analysis. A resting interval of 30 seconds was provided between each trial to minimize fatigue. Participants were allowed to stand up and move during the resting interval. Pressure changes of ± 2 mmHg from the target pressure were allowed to accommodate changes [20].

Results
Twenty-two right-handed individuals were recruited in cLBP group and 24 age matched healthy individuals were recruited in the control group. The sample characteristics of both cohorts are presented in Table 2. There were no group differences for gender, age, height, weight, BMI and educational level. Two cLBP individuals who were unable to maintain 70 mmHg of TA were excluded from the analysis. Therefore, 20 cLBP participants were included in the analyses of TA at the pressure value of 70 mmHg (Table 3). Table 2 Characteristics of the sample cohorts (mean (SD)).

The average EMG amplitudes (AEMG)
During MVIC of TA and MF, compared with pain-free group, cLBP patients showed a significant decrease (P ≤ 0.001). No differences were observed in AEMG at any target pressure value (P > 0.05). Table 3 illustrates the mean and standard deviation of AEMG and MVIC for TA and MF muscles at each target pressure. Correlation between EMG activity and VAS, ODI.

Discussion
This study observed significant association between muscle activities of deep local trunk muscles and pressure measurement of PBU in seated position. The muscle activities of TA and MF during MVIC were lower in the low back pain group than the control group. Muscle activities were significantly higher at each pressure value in the cLBP group than the control group. The slope of the cLBP group was significantly steeper than the control group. The MVIC of MF was negatively correlated with VAS and ODI. TA MVIC was not correlated with VAS or ODI.

MF and TA Muscle Activities in Healthy Controls vs cLBP Patients
Our results indicated that %MVIC of TA and MF were greater and the slope were steeper in participants with cLBP compared with the asymptomatic group. For MF, this was not in line with the study published by Danneels et al. result [36] which suggested that in comparison with the healthy subjects, the chronic low back pain patients displayed significantly lower %MVIC of MF during the coordination exercises. However, findings of our present study were consistent with previous research published by Wang-Price et al. [37] and Ansari et al. [38] which explained the high %MVIC of MF. They suggested that muscle pain could be accompanied by hyperactivity in the back muscles during dynamic conditions, which was called pain adaptation model. In addition, high muscle activity in patients with LBP might be related to muscle spasms [39]. Paraspinal muscles and the connective tissues in the region of the spine contain sensory nerve endings sensitive to changes in position, movement, and tension, which might be initiated by the presence of pain, and some sensory nerve endings related to muscle spasm with increase in activity [40]. Our result that the significant reduction of MVIC of the MF muscle in cLBP group might also explain this phenomenon. The significantly lowered MVIC of MF identified in the present study was consistent with many previous studies [30,35]. However, the mechanism of MVIC reduction is not totally understood, but may be related to pain inhibition which limits the ability to perform maximum muscle contraction. People with cLBP patients had a greater sensitivity to pain [40], thus, we might speculate that cLBP alters spontaneous neuronal activity resulting in muscle EMG activity changes [30]. Additionally, atrophic changes of MF had been confirmed in around 77-80% of LBP cases, especially at the L5-S1 level [41] (the EMG site of MF in our study) which might contribute to lower MVIC in the cLBP group. TA is an important deep muscle that plays a key role in the dynamic control of the lumbar spine [17,18]. The present study observed lower TA muscle activity during MVIC in the LBP group than the healthy group. Hodge et al. studied the contraction timing of TA muscle during upper and lower limb movements in patients with LBP and pain-free controls. A delay of TA muscle contraction relative to the agonist muscle that moved limbs was found in patients with LBP [17,18]. Gildea et al. [42] reported that under contraction status, the thickness of TA was higher in female dancers with cLBP than those without pain. Muscle thickness and contraction ratio were reported to be positively correlated with muscle activity [30]. These data support our finding low muscle activity of the TA during MVIC.
The Difference between TA and MF at Different PBU Pressure in the Two Groups Our results showed that the TA %MVIC was more active than MF %MVIC at 50 mmHg and 60 mmHg in both groups. These findings are consistent with published studies that investigated the relationship between TA and MF in patients with LBP [43]. The study reported that patients who had adequate contraction of multifidus were of 4.5 times likely to be able to contract TA. At the PBU pressure of 70 mmHg, the cLBP group demonstrated almost equal muscle activity in both TA and MF muscles, whereas in the healthy group the %MVIC of MF had more activity than TA. The potential reason may be related to the fatigue of the multifidus muscle. Deep muscle is mostly affected by inhibition reflex which occurs when sensorial input affects muscle activation [44]. According to published literature [40,44,45], sensorial factors influence the recruitment of TA and contribute to MF fatigue. The study by Ramos et al. [46] utilized surface EMG to assess fatigue of MF and PBU to detect activity of TA in patients with LBP. They reported that patients with LBP had difficulties to depress the abdominal wall at the PBU pressure 70 mmHg and higher MF fatigue was observed. Another possible reason is that cLBP patients have reduced flexibility and mobility in the frontal, transverse, and sagittal planes of motion [47]. When TA was contracted at 70 mmHg, there was limited space in the anatomical position [47] that the low back required to complete the motion.

Correlation between EMG activity and VAS, ODI
The present study observed a negative correlation between MVIC of MF and VAS and ODI which was consistent with previous studies [30]. There was no correlation between the MVIC of TA and VAS or ODI. The potential reason was that TA and MF have different roles in maintaining lumbar stability due to their different anatomical structures, different muscle fiber size, different motor unit control properties [16,40,41]. Previous studies had suggested that TA was mainly involved in lumbar stability by contractile increase of abdominal pressure [20,21,24,25], and MF might directly maintain lumbar stability through the thoracolumbar fascia [14,16,39,40,48]. Therefore, compared with TA, MF might be more easily correlated with VAS and ODI. Moreover, maybe TA and MF had different neuromuscular and proprioceptive systems, along with varied changes in biomechanical alignment of spine and developed different models of pain adaptation [49]. However, directly speculating on the connection with neuromuscular control mechanisms and pain was difficult because we know so little about the underlying relationship between brain network and TA and MF muscle activity [43].

Limitations
First, reliability and validity of the PBU and EMG in measuring MF muscle activity in patients with cLBP was not established. Further studies are needed to assess the reliability and validity of this method for evaluating MF. Second, LBP may interfere with the patient's ability to perform maximum muscle contraction. Individuals may therefore not able to perform their "maximum" ability during MVIC due to pain aggravation. The assessor provided detailed instructions and verbal encouragement in the present study as an attempt minimize the impact. The uneven distribution of gender in the sample population was also a limitation. The number of females were significantly more than males.

Conclusions
The study demonstrated the feasibility of using PBU to assess muscle contraction that corresponds with changes of muscle activity as measured by EMG. People with cLBP have reduced ability to perform maximum contraction of the MF and TA muscles when compared to healthy individuals.
People with cLBP have higher muscle activities at each pressure value when compare with healthy individuals. The use of EMG to quantify the extent of how much the PBU activates muscles may provide important information to clinicians and researchers for patients with LBP.

Ethics approval and consent to participate
The study protocol was reviewed and approved by the Human Subjects Ethics Sub-committee of the First Affiliated Hospital, Sun Yat-sen University (Approval number: [2017] C-034). All subjects gave written informed consent. The study was conducted in accordance to the Declaration of Helsinki.