The effects of task execution variables on the musculature activation strategy of the lower trunk during squat lifting

The effects of task execution variables on the musculature activation strategy of the lower trunk during squat lifting

International Journal of Industrial Ergonomics 55 (2016) 77e85 Contents lists available at ScienceDirect International Journal of Industrial Ergonom...

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International Journal of Industrial Ergonomics 55 (2016) 77e85

Contents lists available at ScienceDirect

International Journal of Industrial Ergonomics journal homepage: www.elsevier.com/locate/ergon

The effects of task execution variables on the musculature activation strategy of the lower trunk during squat lifting Iman Vahdat a, Mostafa Rostami b, Farhad Tabatabai Ghomsheh c, *, Siamak Khorramymehr a, Ali Tanbakoosaz d a

Department of Biomedical Engineering, Science and Research Branch, Islamic Azad University, Tehran, Iran Motion Analysis Lab, School of Biomedical Engineering, Amirkabir University of Technology, Tehran, Iran Pediatric Neurorehabilitation Research Center, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran d Faculty of Mechanical Engineering, Abhar Branch, Islamic Azad University, Abhar, Iran b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 14 January 2016 Received in revised form 3 June 2016 Accepted 25 July 2016

The main objective of this study was to investigate the innervation behavior of lower trunk musculature to determine the muscular activation strategy during free dynamic squat lifting. This may clarify how lower trunk musculature activation compliments task execution variables to control motion during labor and industrial lifting tasks. In total, 12 healthy men volunteered to perform symmetric squat lifting of boxes of various masses (4, 8 and 12 kg) at slow and fast speeds. Eight-channel electromyography was performed on two pairs of abdominal (rectus abdominis and external oblique) and lower back muscles (iliocostalis lumborum and multifidus). Movement patterns were extracted using a 3D-linked segment model and a Vicon system. The results indicated that there were significant increases (all p-values < 0.05) in the mean muscle activation of the right and left multifidus and iliocostalis lumborum with increases in the lift speed and box weight. Furthermore, the results indicated that there were significant decreases (all p-values < 0.05) in the time required for the peak activation of the right and left multifidus, iliocostalis lumborum and external oblique with increases in the lift speed and box weight. Finally, the lower trunk musculature activation strategy was revealed to be compatible with different task execution variables, controlling motion in a manner that compensated for the effects of task execution variables. The findings of this study may effectively be applied to ergonomics, particularly to symmetric squat lifting. © 2016 Elsevier B.V. All rights reserved.

Keywords: Squat lifting Lower trunk Muscle activity Electromyography

1. Introduction Weight lifting is commonly performed in various occupational settings. It requires a combination of trunk muscle activation that includes activation of back muscles, which are responsible for trunk extensions and bending moment control (Macintosh and Bogduk, 1986; McGill et al., 1988), and abdominal muscles, which are responsible for flexion moment control at the lumbar spine (Dumas et al., 1988; Gatton et al., 2001). During a lifting task, trunk muscles are activated to initiate, maintain or stop motions (Crisco et al., 1992; McGill, 1997). Knowledge of trunk muscles activation is, therefore, necessary to interpret the relationship between muscle activation and imposed back loading and to determine the muscle activation strategy during weight handling and lifting. * Corresponding author. E-mail address: [email protected] (F.T. Ghomsheh). http://dx.doi.org/10.1016/j.ergon.2016.07.007 0169-8141/© 2016 Elsevier B.V. All rights reserved.

The evaluation of trunk musculature activation and the relative contribution of trunk muscles to spinal loading during weight handling and lifting tasks provides a better understanding of neuromuscular system responses. Surface electromyography (EMG) has been used in numerous studies to investigate various aspects of trunk muscle activation, including physiological (De Luca, 1993; Dedering et al., 2000; Delitto and Rose, 1992; Farina et al., 2004; Henry et al., 1998) and biomechanical aspects (Dolan and Adams, 1993; Macintosh and Bogduk, 1991; Toussaint et al., 1995; Vakos et al., 1994). Several studies have investigated trunk muscle activation during load lifting. Marras and Mirka (1993) conducted EMGs of the lumbar trunk musculature during the generation of low-level trunk acceleration. Fathallah et al. (1997) reported the effects of the complex dynamic characteristics of lifting and lowering on trunk muscle recruitment. Davis and Marras (2000) assessed the relationship between box weight and trunk kinematics. Hwang et al. (2009) investigated lower trunk and lower

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extremity joint kinetics during squat and stoop lifting. Several studies have investigated muscle activation under different conditions, such as isometric and controlled isokinetic conditions (Lavender et al., 1993; Marras and Mirka, 1990, 1993) as well as freedynamic lifting conditions (Granata and Marras, 1995; Hwang et al., 2009; Walsh et al., 2007). Fathallah et al. (1997) reported that the trunk can move freely in an asymmetric or sagittal symmetric plane during a lifting task under free-dynamic and unconstrained conditions. Muscle activation as a result of spinal loading and trunk moments during a lifting task is affected by the amount of load lifted, the lift speed (Davis and Marras, 2000) and other variables, such as lifting frequency (Al-Ashaik et al., 2015; Fox and Smith, 2014; Pinder and Boocock, 2014) and age (Song and Qu, 2014). Davis and Marras (2000) reported that an increase in the amount of load lifted leads to a higher level of muscle activation. Several researchers have reported that an increase in trunk moment is related to increased muscle activation (Dolan and Adams, 1993; Marras and Mirka, 1992; Seroussi and Pope, 1987) and increased spinal loads (Fathallah et al., 1998; Granata and Marras, 1995). Marras and Mirka (1992) reported that an increase in trunk velocity increases muscle activation and spinal loads. Many researchers have reported that increases in sagittal trunk motion and lifting movement speed contributes to increased muscle activity (Kim and Marras, 1987; Marras and Mirka, 1992), increased spinal loading (Granata and Marras, 1995; Marras and Granata, 1997; Marras and Sommerich, 1991) and increased lower back moments (Bush-Joseph et al., 1988; Kingma et al., 2001; Lavender et al., 2003). These findings indicate that muscle activity adjusts to changes in the amount of load lifted and lift speed (Davis and Marras, 2000). Researchers have long sought a better understanding of the function of the neuromuscular system in the lower trunk, particularly the manner in which task execution variables affect muscle activation or the innervation behavior of lower trunk musculature during weight handling and lifting tasks. A qualitative investigation of muscular innervation behavior may help determine the muscular activation strategy, one of numerous unknowns with regard to human physiology, and may clarify how muscle activation compliments task execution variables to direct motion in the manner desired. Moreover, the qualitative investigation of muscular innervation behavior may benefit our understanding of the human motor control system, one of the most important scientific fields of study with regard to the human body. Previous works have quantitatively investigated trunk muscle activation under different lifting conditions. However, there are few qualitative studies regarding the innervation behavior of lower trunk muscles during weight handling and lifting tasks. Therefore, the purpose of the present study is to investigate the muscular activation strategy of lower trunk muscles during lifting. The trunk can move freely in a sagittal symmetric plane during a lifting task under free-dynamic conditions. Moreover, among common lifting techniques (squat and stoop), many researchers have suggested squat lifting for lifting activities (De Looze et al., 1993; Duplessis et al., 1998; Hwang et al., 2009; Welbergen et al., 1991). Compared to stoop lifting, squat lifting is an activity that involves multiples joints and involves more collaboration between the trunk and lower body joints. Hence, the specific objective of this study is to elucidate the innervation behavior of the lower trunk musculature in order to determine the body's muscular activation strategy during symmetric squat lifting. The results obtained may help clarify how lower trunk musculature activation compensates for the effects of task execution variables in order to enable the motion desired during labor and industrial squat lifting tasks. The EMG curves of muscle recruitment patterns have been used qualitatively to investigate the innervation behavior of the lower trunk

musculature. The mean normalized EMG and the time required to reach peak muscle activation constitute the quantitative parameters by which this study investigates the innervation behavior of lower trunk muscles. 2. Materials and methods 2.1. Subjects In total, 12 healthy male subjects with no history of back musculoskeletal disorders or back pain volunteered to perform various lifts. Written consent was obtained from all participants (Table 1). The load levels (4, 8 and 12 kg box weights) were equal for all subjects in this study, and inclusion and exclusion criteria were based on the participants' body mass indices (BMIs) and demographics. Based on the load levels employed, the participants' BMI indices were determined to be in the average range. All procedures and ethical principles pertaining to this study were in accordance with the World Medical Association Declaration of Helsinki and were approved by the research ethics committee of the Department of Biomedical Engineering at the Science and Research Branch of Islamic Azad University. 2.2. Lifting tasks Subjects lifted a box (32 [width]  40 [length]  25 [height] cm, containing handles on either side), which was placed symmetrically in front of their feet, to an upright symmetrical standing position using the symmetric squat technique. Lifts of 4-, 8- and 12-kg boxes were performed at slow speed (~3.3 s duration) and fast speed (~1.1 s duration), as determined by a metronome. The load levels were similar to load distributions observed in industrial tasks (Marras et al., 1995). The speed at which the boxes were lifted differed so that the effects of lift speed changes on the innervation behavior of each participant's lower trunk muscles could be investigated. Each participant's bended lumbar angle was adjusted using a goniometer so that each subject assumed the same body posture when lifting was initiated. Each lift was repeated twice, with a rest interval of 2 min between lifts. The order of performances was randomized to prevent any effects of training or fatigue. The subjects were asked to repeat the experiments one week after the first testing session to ensure reliability. In order to familiarize subjects with the experiment, a training session was held four days before the first test. 2.3. Electromyography An eight-channel EMG (DataLOG MWX8, Biometrics LTD., lon, UK) of the lower back muscles and abdominal muscles was used to analyze muscle activity. Before each experiment, surface EMG electrodes were attached to the participant's carefully cleaned skin as follows. Bipolar silveresilver surface electrodes (with a diameter of 10 mm and an inter-electrode distance of 20 mm) were placed over two pairs of lower back muscles as extensors (multifidus and iliocostalis lumborum) and two pairs of abdominal muscles as

Table 1 Mean and standard deviations of the variable ages, weights, heights and BMIs of participants in this study. Variable

Mean ± SD

Age (years) Weight (kg) Height (cm) BMI (kg/m2)

28.5 ± 3.57 66.62 ± 3.6 170 ± 2.64 23.12 ± 1.65

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flexors (external oblique and rectus abdominis). Because multifidus is a deep muscle that is covered by superficial muscles, crosstalk could occur between muscles during signal recording. To minimize such crosstalk, the following steps were taken. Electrodes were placed carefully within the borders of the muscles and parallel to the muscle fibers. The skin impedance was measured and was accepted if it was less than 5000 U. Multifidus electrodes were placed at the L5 level, parallel to the line between PSIS and the L1e2 interspinous space, at which the multifidus fibers are shallower, as many researchers believe multifidus activation can be detected by surface EMG (Ekstrom et al., 2008; McGill and Sharrott, 1990; NG et al., 2002). The iliocostalis lumborum electrodes were placed at the L2 level, parallel to the line connecting the posterior superior iliac spine (PSIS) to the lateral border of the muscle at the 12th rib. External oblique muscle electrodes were placed just below the rib cage, along the line connecting the most inferior point of the costal margin to the contralateral pubic tubercle. Rectus abdominis electrodes were placed 1 cm above the umbilicus and 2 cm lateral to the midline. The procedure used for EMG testing of back and abdominal muscles was consistent with that of NG et al. (2001, 2002). EMG signals were band-pass filtered at 10e500 Hz and sampled at 1000 Hz (Shrout and Fleiss, 1979). EMG signals were then rectified, and the root mean square value was calculated using a time constant of 20 ms. To normalize the EMG data, the maximum voluntary contractions (MVCs) in the extension (for back muscles) and the flexion and lateral flexion on both sides (for abdominal muscles) were measured twice for 5 s in each subject with a 2-min rest interval between trials. For the MVCs of the extensors, subjects were asked to lie in a prone position with their hands beside their bodies and their legs extended. Resistance was applied to the upper thoracic area in the direction of the trunk flexion. For the external obliques on the right and left sides, subjects were asked to assume a supine position with knees flexed and hands behind their heads. Subjects flexed their trunk and rotated to the right and left. Resistance was applied at the shoulders in the trunk extension and right and left rotation directions. For the MVC of the rectus abdominis, subjects were asked to assume a partial sit-up position with their hands behind their heads and knees flexed. Subjects flexed their abdominal muscles, and resistance was applied to their shoulders in the trunk extension direction. Subjects were asked to gradually increase the force in order to reach an absolute maximum force. Contractions were executed in a randomized order, and one warmup trial was performed before each test. The subjects were asked to exert their maximum effort and avoid jerky contractions during the MVC tests. To obtain high reliability in the EMG measurements, the same procedures were reproduced exactly in the second testing session. 2.4. Motion analysis and kinematic data collection Movement patterns were described using a dynamic threedimensional linked segment model. Kinematics data were collected at 100 Hz using a Vicon system (Vicon-460 Motion System Ltd., LA, USA) and 27 passive reflective markers, which were placed on the skin on the right and left sides of the body, according to the Helen Hayes marker set-up (Tabakin and Vaughan, 2000). A 13segment body model (for whole body), consisting of feet, lower legs, upper legs, pelvis, trunk, head plus neck, upper arms and forearms plus hands, was used to define the positions of the following joints: the fourth metatarsophalangeal joint, the ankle joint (the distal part of the lateral malleolus), the knee joint (epicondylus lateralis), the hip joint (greater trochanter), the L5eS1 joint, the first thoracic vertebra (C7eT1), the ear channel (the head), the glenohumeral joint, the elbow joint (epicondylus

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lateralis) and the wrist joint (ulnar styloid). 2.5. Data analysis To obtain the mean normalized EMG (MNEMG) value and a clear linear envelope curve showing the innervation behavior of muscle recruitment, the calculated root mean square values of the EMG data for each muscle were normalized with respect to the MVC. Because the MNEMG value represents the mean level of normalized muscle activity during a particular movement, this value was used to compare the activity levels of each individual lower trunk muscle as a result of different lifts; this procedure is consistent with that of Fathallah et al. (1997) and NG et al. (2002). Finally, the EMG curves were time normalized (ranging from 0 to 100%). To outline the mean trends of the EMG curves of muscle recruitment patterns during task executions, the time required to reach peak muscle activation (TTP value) was calculated for each lift. The independent variables in this study included the box weight and lift speed, and the dependent variables were the MNEMG and TTP values for the lower trunk muscles during six different lifts. To extract the movement pattern, kinematics data were input into the linked segment model. Joint angles were defined in the sagittal plane (Fig. 2). The ankle joint angle was defined as the angle between the line through the ankle and knee joints and the vertical line. The knee joint angle was defined as the angle between the line through the knee and ankle joints and the line through the knee and hip joints. The hip joint angle was defined as the angle between the line through the hip and knee joints and the line through the hip and L5eS1 joints. For the lumbar angle, the angle between the line through the L5eS1 and hip joints and the line through the L5eS1 and T1 joints was measured, consistent with Van der Burg et al. (2000). An electrical switch was placed between the box and ground to define the ‘zero’ time point for all lifts. The lift start time, at which the lumbar angle was approximately 85 , was defined by the activation of the electrical micro-switch. Moreover, the lift end, at which point the trunk was fully extended, was defined by a constant lumbar angle (approximately 27 ). All calculations and data analyses were performed in the sagittal plane using MATLAB-R2010 software. 2.6. Statistical analysis Two-way repeated measures ANOVA was applied to the data to evaluate the effects of box weight and lift speed on the MNEMG and TTP values obtained as well as to detect any interactions between lift speed and box weight. In addition, two-way repeated measures ANOVA was applied to the kinematics data to test the effects of box weight and lift speed on the angular positions of lower extremity joints. The means obtained were significantly different, with pvalues less than 0.05. Reliability was examined using intra-class correlation coefficients (ICCs) (Shrout and Fleiss, 1979). Statistical analyses were conducted using the SPSS statistical package (version 16), and ICCs were interpreted according to Domholdt (2005). 3. Results ICC reliability values for the MNEMG, TTP and joint angular positions were calculated for each lift. The best reliabilities were obtained for MNEMG and TTP in the following four muscles: right and left multifidus (0.81 < all ICCs < 0.92) and right and left iliocostalis lumborum (0.8 < all ICCs < 0.89). High reliabilities were also observed in the remaining four muscles, including the following: right and left rectus abdominis (0.74 < all ICCs < 0.86) and right and left external oblique (0.73 < all ICCs < 0.86). The ICC

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reliability values pertaining to the angular positions of joints revealed high reliabilities for all lower extremity joints for all box weights lifted and at both lift speeds (0.87 < all ICCs < 0.94). Fig. 1 shows the MNEMG and TTP values obtained for eight trunk muscles using six different lifts. Table 2 presents the two-way repeated ANOVA results, which indicate significant increases (all p-values < 0.05) in the MNEMG values of the right and left multifidus and the iliocostalis lumborum with increases in lift speed and box weight. Moreover, significant interactions (all p-values < 0.05) were detected between lift speed and box weight. According to the results in Table 2, insignificant increases (all p-values > 0.05) were observed in the MNEMG values of the right and left rectus abdominis and the external oblique as the box weight increased. The results in Table 2 indicate significant decreases (all pvalues < 0.05) in the TTP values of the right and left multifidus, the iliocostalis lumborum and the external oblique as lift speed and box weight were increased. Significant decreases (all p-values < 0.05) in the TTP values of the right and left rectus abdominis accompanied increases in lift speed. Moreover, significant interactions (all pvalues < 0.05) were detected between lift speed and box weight. The activation level of rectus abdominis increased with

increases in box weight and lift speed, while increasing the lift speed decreased the activation level of the external obliques when higher loads were used (8 and 12 kg masses) (Fig. 1). The angular positions of the lower extremity joints are represented in Fig. 2. The angular positions of joints at time points corresponding to 25%, 50% and 75% of the total movement time were determined so that the effects of lift speed and box weight on the angular positions of joints could be evaluated. Two-way repeated measures ANOVA results showed significant changes (all pvalues < 0.05) in knee and L5eS1 angular positions with increased lift speed. Furthermore, insignificant changes (all p-values > 0.05) were detected in the angular positions of all joints as the box weight was increased. Therefore, excepting the knee and L5eS1 joints, every joint investigated displayed approximately the same angular position pattern as the lift speed increased. Based on the lumbar angular positions (Fig. 2) that occurred during fast lifting, the lumbar spine was extended from the beginning of the movement; on the other hand, during slow lifting, the lumbar spine became more flexed after the beginning of the movement and then extended until the end of the movement. Thus, different movement patterns were observed for slow versus fast lifting.

Fig. 1. Muscular innervation profiles of the four pairs of lower trunk muscles during squat lifting of three masses (4, 8 and 12 kg) at two lift speeds (slow and fast). The data shows the MVC normalized mean EMG (MNEMG) and the time required to reach peak muscle activation (TTP). MU: multifidus, IL: iliocostalis lumborum, RA: rectus abdominis, EO: external oblique. r: right side muscle, l: left side muscle.

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Table 2 The results of two-way repeated measure ANOVA, which was applied to the data to evaluate the effects of box weight and lift speed on MNEMG and TTP values as well as to detect any interactions that may occur between lift speed and box weight. Dependent variable

MNEMG

Independent variable

Lift speed Box weight Interaction

TTP

Lift speed Box weight Interaction

Muscle MU-r

MU-l

IL-r

IL-l

RA-r

RA-l

EO-r

EO-l

P ¼ 0.002 F ¼ 9.84 P ¼ 0.021 F ¼ 7.48 P ¼ 0.001 F ¼ 20.2

P ¼ 0.000 F ¼ 8.12 P ¼ 0.014 F ¼ 7.12 P ¼ 0.003 F ¼ 23.23

P ¼ 0.01 F ¼ 5.96 P ¼ 0.001 F ¼ 11.34 P ¼ 0.000 F ¼ 19.03

P ¼ 0.012 F ¼ 6.12 P ¼ 0.000 F ¼ 10.22 P ¼ 0.000 F ¼ 18.85

P ¼ 0.488 F ¼ 0.56 P ¼ 0.286 F ¼ 1.81 P ¼ 0.733 F ¼ 0.27

P ¼ 0.471 F ¼ 0.48 P ¼ 0.266 F ¼ 1.68 P ¼ 0.681 F ¼ 0.22

P ¼ 0.61 F ¼ 0.17 P ¼ 0.89 F ¼ 0.092 P ¼ 0.198 F ¼ 3.44

P ¼ 0.58 F ¼ 0.13 P ¼ 0.621 F ¼ 0.08 P ¼ 0.210 F ¼ 4.56

P ¼ 0.000 F ¼ 23.72 P ¼ 0.016 F ¼ 15.22 P ¼ 0.000 F ¼ 33.24

P ¼ 0.000 F ¼ 24.1 P ¼ 0.011 F ¼ 14.77 P ¼ 0.000 F ¼ 36.87

P ¼ 0.000 F ¼ 19.26 P ¼ 0.01 F ¼ 13.12 P ¼ 0.000 F ¼ 38.54

P ¼ 0.000 F ¼ 18.95 P ¼ 0.009 F ¼ 11.76 P ¼ 0.000 F ¼ 32.12

P ¼ 0.000 F ¼ 19.3 P ¼ 0.122 F ¼ 8.21 P ¼ 0.241 F ¼ 13.9

P ¼ 0.000 F ¼ 20.32 P ¼ 0.141 F ¼ 9.68 P ¼ 0.178 F ¼ 17.33

P ¼ 0.01 F ¼ 31.3 P ¼ 0.019 F ¼ 45.43 P ¼ 0.000 F ¼ 52.88

P ¼ 0.012 F ¼ 32.32 P ¼ 0.011 F ¼ 42.48 P ¼ 0.000 F ¼ 59.12

MNEMG: mean normalized EMG, TTP: time to peak muscle activation. MU: multifidus, IL: iliocostalis lumborium, RA: rectus abdominis, EO: external oblique, r: right, l: left. Significant differences are shown in bold. The significance level ¼ 0.05 are shown in italics.

Fig. 2. Curve patterns of the angular position of the lower joints in response to lifting at fast and slow speeds. The bars indicate one standard error of the mean. The box was lifted from ground level (at a lumbar angle of approximately 85 ) to full extension of the trunk.

Fig. 3 shows the EMG curve patterns obtained for the activity of lower trunk muscles during different lifts. During fast lifting, the activity level of the extensors peaked at the beginning of the movement (at a lumbar angle of approximately 85 ), after which the activity level decreased gradually. On the other hand, during slow lifting, the extensors achieved peak activity between 15% and 35% of the total movement time (at a lumbar angle of 86  Ө < 88 ), after which their activity levels decreased (Fig. 3). During fast lifting, excepting the external oblique during lifting of the 4-kg box, the activity level of the flexors peaked at the beginning of the movement (at a lumbar angle of approximately 86.5 ), after which their activity levels decreased. During slow lifting, the flexors obtained peak activity between 25% and 40% of the total

movement time (at a lumbar angle of 86 < Ө < 88 ), after which their activity levels decreased. 4. Discussion 4.1. Mean normalized EMG The results of the present study provide information regarding the functions of various muscles when executing different symmetric free dynamic squat lifts. The muscles investigated demonstrated a variety of activity levels and recruitment patterns throughout the experiments. The most active muscles were the extensor muscles, which demonstrated the highest activity levels

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Fig. 3. MVC normalized EMG curve patterns of the four pairs of lower trunk muscles during squat lifting of three masses (4, 8 and 12 kg) at two lift speeds (slow and fast). The bars indicate one standard error of the mean. MU: multifidus, IL: iliocostalis lumborum, RA: rectus abdominis, EO: external oblique.

and the greatest alterations in EMG curves pertaining to muscle recruitment patterns, in agreement with previous studies (Fathallah et al., 1997; Marras and Mirka, 1990). Although all lifts in the present study were executed under symmetric conditions, the role of flexor muscles was not as significant as the role of extensors. By contrast, Fathallah et al. (1997) emphasized the importance of flexors in the asymmetric condition. Based on previous studies (Dolan and Adams, 1993; Kingma et al., 2001; Lavender et al., 2003; Marras and Sommerich, 1991), we anticipated that the MNEMG values of most of the trunk muscles would increase with increasing box weight and lift speed. Although the load levels (4, 8 and 12 kg masses) in this study were similar to load distributions observed in industrial tasks, the extensors sensitivity to loads in this range appeared to be higher than that of flexor muscles, a result we also anticipated due to the role of extensors in trunk extension and controlling the bending moment. Increasing the lifting speed increased the MNEMG values of most of the trunk muscles and particularly the extensor muscles, which is

consistent with previous studies (Fathallah et al., 1997; Marras and Mirka, 1992). The sensitivity of the extensor muscles to lifting speed appeared to be higher than that of the flexor muscles, perhaps for the same reason discussed above. The effects of increased box weight and lift speed on the activation level of the external oblique muscle were undefined (Fig. 1), as no significant changes were observed in the innervation behavior of this muscle. This may be related to the influence of intra-abdominal pressure (IAP), which has reportedly demonstrated a high correlation with activation of the abdominal musculature (McGill and Sharrott, 1990). Unlike the external oblique muscle, the rectus abdominis muscle exhibited increased activation levels as the box weight and lift speed were increased (Fig. 1). Given the relationship between IAP and abdominal musculature activation, we cannot conclusively explain the observed alteration in abdominal muscle activation. Abdominal muscle activation increases the mechanical loading on the spine and generates a flexion torque during lifting tasks (Van der Burg

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et al., 2000). Van der Burg et al. (2000) proposed that activation increases in order to maintain and adjust trunk stability. Thomas et al. (1998) reported increased abdominal muscle activity when an unexpected perturbation was imposed during standing. Oddsson et al. (1999) reported the same finding when backward support perturbations were imposed during lifting. 4.2. EMG curve patterns TTP values (Fig. 1), which represent the time required to reach peak muscle activation, indicate that the flexors reached peak activation after the extensors in most lifts. Van der Burg et al. (2000) have suggested that a burst of flexors activation inhibits performance of the lifting task because this burst of activation decreases the extension moment. Tesh et al. (1987) have reported that increased flexors activation might stabilize the lumbar spine, which might prevent increased extensor activation, maintaining and stabilizing the trunk. Increases in both box weight and lift speed significantly and intensively reduced the TTP values of most of the trunk muscles investigated herein. At the higher lift speed, extensors were stimulated at peak activation at the start of lifting, demonstrating the influence of the speed of motion on the innervation behavior of extensors during task performance. Increasing the lift speed resulted in different movement patterns, as demonstrated by alterations in the angular positions of the knee and lumbar spine (Fig. 2). Thus, the decrease in TTP values of the extensors in response to increased lift speed appears to demonstrate the influence of lift speed on movement performance. As mentioned previously, during fast lifting, the lumbar spine was extended from the beginning of the movement, at which point the extensors were at their highest activation levels; on the other hand, during slow lifting, the lumbar spine became more flexed after the movement began, after which it extended until the end of the movement. This may explain the decrease in the TTP values of the extensors observed when the lift speed was increased. Previous studies have reported increased shear and compressive forces in knee and tibio-femoral joints at higher movement speeds (Dahlkvist et al., 1982; Hattin et al., 1989) and higher loads (Sahli et al., 2008). Hay et al. (1983) found a relationship between an increased box weight and spinal curvature. A linear correlation between spinal compression, box weight and degree of hyperextension was reported by Walsh et al. (2007) at higher loads as a compensatory action to direct motion as desired. Fathallah et al. (1997) reported the compensatory role of the joints in effecting high-speed movement during lifting under unconstrained conditions. Rossi et al. (2014) reported changes in trunk muscle activation to maintain stability during the execution of different exercises. These findings emphasize the compensatory actions of joints and muscles to achieve proper spinal alignment and to prevent imposing excessive forces on certain body regions during lifting under unconstrained conditions. Based on these findings and considering previous findings regarding the relationship between trunk kinematics, box weight, muscle activity and spinal loading (Bush-Joseph et al., 1988; Davis and Marras, 2000; Kingma et al., 2001; Lavender et al., 2003), we may deduce that muscle activity can be altered to compensate for changes in box weight and lift speed. The different movement patterns observed in response to slow versus fast lifting may represent compensatory actions on the part of the knee and lumbar spine in response to high-speed movement (excessive forces and increased extension moment). During fast lifting, the knee and lumbar spine extended much more rapidly, apparently to provide an increased extension moment, besides the lower joints. Considering the compensatory actions of

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the knee and lumbar spine in response to high-speed movement, decreases in the TTP values of the extensors as a result of increased lift speed appears justified. Although insignificant changes were detected in the angular positions of all joints in response to increased box weight, the TTP values of most of the lower trunk muscles decreased significantly. Considering the compensatory actions of muscles as well as the alterations in muscle activity in response to increased spinal loading with higher load lifting, trunk extensors may reach peak activation much more rapidly, in order to compensate for the effects of a higher load (excessive force and increased extension moment) as well as to provide an increased extension moment, besides the lower joints (Fig. 1 and Table 2). This may explain the decrease observed in the TTP values of extensors as a result of increasing the box weight. A greater increase in the box weight results in a greater increase in the excessive force and in the extension moment, which ultimately results in more rapid activation of the extensors as a compensatory action. This may explain the significant decrease observed in the TTP values of the extensors under conditions of higher load lifting. Based on the findings described above, it seems that the lumbar extensors reach peak activation much more rapidly in order to compensate for the effects of higher loads and higher movement speeds under conditions of higher load lifting and higher speed lifting, respectively. Given that increased flexor activation may stabilize the lumbar spine, the flexors may reach peak activation more quickly in order to stabilize the trunk, while the extensors play compensatory roles. This may explain the decrease in the TTP values of flexors that occurs in response to increases in lift speed and box weight. According to Figs. 1 and 3, increases in box weight and lift speed altered lower trunk musculature activities, demonstrating the effect of external loading on the innervation behavior of the lower trunk musculature during squat lifting. EMG curves and movement patterns further elucidated the response of lower trunk musculature activation to the effects of task execution variables in order to control motion. 4.3. Interaction between lift speed and box weight Two-way repeated measures ANOVA results (Table 2) indicate significant interactions between lift speed and box weight with regard to MNEMG and TTP values, indicating that the relationship between each of these interacting variables (lift speed and box weight) and muscle activity depends on the value of the other interacting variable. Inertial force is numerically the product of mass and acceleration of the center of gravity of a system (subject plus box). Thus, changes in the mass and speed of the system are factors that affect muscle activity, the interaction between lift speed and box weight appears to refer to the effect of the inertial force of the system on muscle activity during symmetric squat lifting. As previously discussed, both lift speed and box weight influenced the MNEMG and TTP values of most of the lower trunk muscles. Therefore, the interaction between these variables, which appears to refer to the effect of the inertial force of the system, can influence the MNEMG and TTP values of the lower trunk muscles. 5. Conclusions The findings reported herein provide further insight into the innervation behavior and activation strategy of the lower trunk musculature during squat lifting tasks and, furthermore, reveal how lower trunk muscle innervation is affected by box weight and lift speed during task performance and how lower trunk muscles

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are compatible with the effects of task execution variables. Finally, the activation strategy of the lower trunk musculature is revealed to be compatible with different task execution variables, compensating for the effects of these task execution variables to control motion. 6. Practical application The findings of the present study can be effectively applied in ergonomics relating to symmetric squat lifting. Based on these findings, the activation of lower trunk muscles during squat lifting is affected by the weight of the box and the movement speed and inertial force of the system. Clearly, increases in the box weight and movement speed increase and decrees MNEMG and TTP values, respectively. Otherwise, abnormal muscular function is implied. These findings also demonstrate the compensatory actions of joints and muscles for the purpose of controlling movement. The results reported herein may inform and help subjects to achieve proper motion in order to prevent jerky movements and excessive forces on the lower joints during risky squat lifting tasks in industrial and labor applications. Based on the MNEMG and TTP values of the lower trunk musculature during squat lifting, clinicians may be able to evaluate subjects' muscular functions. Understanding the natural EMG curve patterns and innervation behavior of the lower trunk musculature during squat lifting performance (Fig. 3), clinicians may be able to diagnose abnormal and jerky muscular contractions that may have be present during risky industrial or labor lifting tasks. For instance, with access to the EMG curve pattern and TTP data, undesirable peaks can be detected within EMG curve patterns and specified as indications of jerky movements. 7. Limitations The narrow range of BMI indices, sexuality, age and box masses and lift speeds were limitations of this study. All participants in this study were young males and their BMI indices were limited to a specific range. In addition, the box masses and lift speeds employed fell within limited ranges. The results might have differed if the participants were not young males or if their BMI indices were limited to a different range. Furthermore, the findings of the study may be valid only for the determined box masses and lift speeds. The experiments in this study were conducted utilizing only symmetric squat lifting conditions. Other lifting conditions, such as asymmetric lifting, may cause different innervation behavior in the muscles investigated. Conflict of interest We confirm that no potential conflict of interest has been reported with regard to this article. Acknowledgments The authors wish to thank Professor Mohammad Parnianpour for his participation in discussions, and all the subjects who participated in this study. References Al-Ashaik, R.A., Ramadan, M.Z., Al-Saleh, K.S., Khalaf, T.M., 2015. Effect of safety shoes type, lifting frequency, and ambient temperature on subject's MAWL and physiological responses. Int. J. Ind. Ergon. 50, 43e51. Bush-Joseph, C., Schipplein, O., Andersson, G.B., Andriacchi, T.P., 1988. Influence of dynamic factors on the lumbar spine moment in lifting. Ergonomics 31, 211e216. Crisco, J.J., Panjabi, M.M., Yamamoto, I., Oxland, T.R., 1992. Euler stability of the

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